Ele12398 PDF

Ecology Letters, (2014) doi: 10.1111/ele.
12398
REVIEW AND
SYNTHESIS Islands as model systems in ecology and evolution: prospects
fifty years after MacArthur-Wilson
Abstract
Ben H. Warren,1,2,3* Daniel The study of islands as model systems has played an important role in the development of evolu-
Simberloff,2 Robert E. Ricklefs,4 tionary and ecological theory. The 50th anniversary of MacArthur and Wilson’s (December 1963)
Robin Aguilee,5 Fabien L. article, ‘An equilibrium theory of insular zoogeography’, was a recent milestone for this theme.
Condamine,6 Dominique Gravel,7 Since 1963, island systems have provided new insights into the formation of ecological communities.
le
He ne Morlon,8 Nicolas Here, building on such developments, we highlight prospects for research on islands to improve our
Mouquet,9 James Rosindell,10 understanding of the ecology and evolution of communities in general. Throughout, we emphasise
Juliane Casquet,5 Elena Conti,1
how attributes of islands combine to provide unusual research opportunities, the implications of
Marıa
Josselin Cornuault,5 Jose
which stretch far beyond islands. Molecular tools and increasing data acquisition now permit re-
ndez-Palacios,11 Tomislav
assessment of some fundamental issues that interested MacArthur and Wilson. These include the
Ferna
formation of ecological networks, species abundance distributions, and the contribution of evolu-
Hengl,12 Sietze J. Norder,13
tion to community assembly. We also extend our prospects to other fields of ecology and evolution
Kenneth F. Rijsdijk,13 Isabel
– understanding ecosystem functioning, speciation and diversification – frequently employing assets
Sanmartın,14 Dominique
of oceanic islands in inferring the geographic area within which evolution has occurred, and poten-
Strasberg,3 Kostas A. Triantis,15,16
tial barriers to gene flow. Although island-based theory is continually being enriched, incorporating
Luis M. Valente,17 Robert J. non-equilibrium dynamics is identified as a major challenge for the future.
Whittaker,16 Rosemary G.
Gillespie,18 Brent C. Emerson19 Keywords
and Christophe Th ebaud5,20 Community assembly, diversification, ecosystem functioning, genomics, island biogeography,
islands as model systems, speciation.
Ecology Letters (2014)
paper, ‘An equilibrium theory of insular zoogeography’, R.

INTRODUCTION
H. MacArthur and E. O. Wilson took their first step in a
Fifty years ago, two young ecologists were disheartened by landmark endeavour both to add statistical rigour to com-
the descriptive and old-fashioned nature of their field, the munity ecology and to establish a conceptual foundation for
importance of which was becoming overshadowed by revo- further work. Inspired by previous advances in biology
lutionary advances in molecular biology. In their 1963 using insular systems, they recognised the utility of island
1 12
Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008, ISRIC–World Soil Information, 6700 AJ, Wageningen, The Netherlands
13
Zurich, Switzerland Institute for Biodiversity and Ecosystem Dynamics, Institute for Interdisci-
2
Department of Ecology and Evolutionary Biology, University of Tennessee, plinary Studies, University of Amsterdam, Science Park 904, 1098XH,
Knoxville, TN, 37996, USA Amsterdam, The Netherlands
3
UMR PVBMT, Universite de La Re
union-CIRAD, 7 chemin de l’IRAT, Ligne nico, RJB-CSIC, Plaza de Murillo 2, 28014, Madrid, Spain
Real Jardın Bota
14
union, France
Paradis, 97410, Saint Pierre, Re 15
Department of Ecology and Taxonomy, Faculty of Biology, National and
4
Department of Biology, University of Missouri at St. Louis, 8001 Natural Kapodistrian University, Athens, 15784, Greece
16
Bridge Road, St. Louis, MO, 63121, USA Oxford University Centre for the Environment, South Parks Road, Oxford,
5
Biologique, UMR 5174 CNRS-Universite
Laboratoire Evolution & Diversite OX1 3QY, UK
17
Paul Sabatier-ENFA, 31062 Toulouse Cedex 9, France Unit of Evolutionary Biology/Systematic Zoology, Institute of Biochemistry
6
CNRS, UMR 7641 Centre de Mathematiques Applique es (Ecole Polytech- and Biology, University of Potsdam, Karl-Liebknecht-Strasse 24-25, 14476,
nique), Route de Saclay, 91128, Palaiseau, France Potsdam, Germany
7
partement de Biologie, Universite
De du Que bec a
Rimouski 300, Alle
e des 18
Division of Organisms and Environment, University of California, Berkeley,
Ursulines, Rimouski, QC, G5L 3A1, Canada CA, 94720, USA
8
rieure (IBENS), UMR CNRS 8197,
Institut de Biologie de l’Ecole Normale Supe 19
Island Ecology and Evolution Research Group, Instituto de Productos
46 rue d’Ulm, 75005, Paris, France nchez 3, La
Naturales y Agrobiologıa (IPNA-CSIC), C/Astrofısico Francisco Sa
9
Institut des Sciences de l’Evolution, UMR 5554, CNRS, Univ. Montpellier 2, CC Laguna, 38206, Tenerife, Canary Islands, Spain
ne Bataillon, 34095, Montpellier Cedex 05, France
065 Place Euge 20
CESAB / FRB, Domaine du Petit Arbois, Av Louis Philibert, Aix-en-Provence,
10
Department of Life Sciences, Imperial College London, Silwood Park 13100, France
Campus, Ascot, Berkshire, SL5 7PY, UK *Correspondence: E-mail: [email protected]
11
Island Ecology and Biogeography Group, Instituto Universitario de Enfer-
blica de Canarias (IUETSPC), Universidad de La
medades Tropicales y Salud Pu
Laguna, Tenerife, Canary Islands, Spain
© 2014 John Wiley & Sons Ltd/CNRS

2 B. H. Warren et al. Review and Synthesis
Box 1 Island biogeography theory: a summary of MacArthur and Wilson’s main hypothesis, and some definitions
IBT was inspired by two patterns of species richness that had been documented by the early 1960s – the species–area and spe-
cies–distance relationships. The first of these describes the positive relationship between the area of habitat considered, and the
number of species found within that area. This may be the oldest recognised ecological pattern, descriptions dating back to the
mid-18th century (see Triantis et al. 2012). The second pattern describes the reduction in species richness of islands with dis-
tance from the source of colonisation. It had been expressed qualitatively by many authors prior to IBT, notably E. Mayr and
P. J. Darlington (see MacArthur & Wilson 1963).
MacArthur & Wilson (1963) noted that the low species richness of remote islands had previously been attributed to the length
of time available for species to colonise and their chances of reaching a remote island in that time. Inspired by density-depen-
dent regulation of population sizes (Lack 1954), they proposed that island species diversity should rather be viewed as a diver-
sity-dependent dynamic balance between immigration and extinction, and they made two assumptions concerning these
processes. They assumed that the immigration rate for an island falls as the number of species on the island increases and that
the rate of extinction of species increases as the number of species increases. Together, these two assumptions imply that diver-
sity will tend towards equilibrium (Fig. 1).
At equilibrium, the number of species on the island stabilises, with the rate of immigration of new species balanced by the
rate of extinction (Fig. 1). Based on this equilibrium, MacArthur & Wilson (1963) made two principal assumptions (Fig. 1) con-
cerning the effects of island area and its distance from the source of colonisation, other things being equal. First, near islands
will have higher immigration rates than far islands. Second, small islands will have higher extinction rates than large islands.
Provided that the immigration and extinction curves are monotonic, and regardless of their precise shape, two main predictions
can be drawn from these assumptions, other things being equal. First, near islands have more species than far islands. Second,
large islands have more species than small islands.
Although MacArthur and Wilson were not the first to have such ideas (see Lomolino & Brown (2009) for Eugene G. Mun-
roe’s earlier and independent work), they were the first to develop and publicise them. We refer to this model as Core IBT, to
distinguish it clearly from other ideas that MacArthur and Wilson developed in both the 1963 paper, and final six chapters of
their 1967 monograph (MacArthur & Wilson 1967). Exemplifying the importance of this distinction, although Core IBT does
not incorporate speciation, MacArthur & Wilson (1963, 1967) nonetheless provided detailed insights as to the conditions under
which speciation should occur on islands (Gillespie & Baldwin 2010). Likewise, although Core IBT does not consider species
identity, this identity and the ecological differences between species are key to ideas expressed in chapters 5 and 7 of the 1967
monograph.
biotas as providing discrete, manageable and replicated bution of island studies to our understanding of fundamental
microcosms of biological communities in general. processes in ecology and evolution, the importance of which
Two different conclusions can be drawn regarding the leg- stretch far beyond islands (but see Grant 1998). Our aim in
acy of MacArthur & Wilson’s (1963) theory (herein ‘Island this review is to provide a forward-looking view of prospects
Biogeography Theory’, IBT; Box 1; Fig. 1). On the one
hand, viewed as a strict explanatory model for patterns of (a) (b)
species diversity, appreciation of its utility has been mixed
(e.g. Gilbert 1980; Williamson 1989; Schoener 2010). Despite Island area effect Island distance effect
being a good predictor of diversity patterns, the hypothesis
of equilibrium, as originally defined, may be unfalsifiable Small Near
Rate
(Simberloff 1976). On the other hand, MacArthur and Wil-

Rate
son’s broader aim – using islands as model systems to

develop a conceptual framework for their field – has been
an unquestionable success. In the 50 years since IBT’s con- Large Far
ception, it has spawned or inspired many ecological and
evolutionary models, not all of which concern islands. Like-
Number of species Number of species
wise, the literature stemming from MacArthur & Wilson
(1963, 1967) is colossal. It includes reviews of the validity Immigration rate Extinction rate
of the core model (e.g. Simberloff 1976; Gilbert 1980;
Schoener 2010), island biogeography (e.g. Whittaker and
Figure 1 The Core IBT model (see Box 1 for definition), illustrating
Fern andez-Palacios 2007) and the wider legacy of their work to
MacArthur & Wilson’s (1963, 1967) assumptions regarding the following:
ecology and evolutionary biology (e.g. Losos & Ricklefs 2010) (a) the effect of island area on extinction rate, and (b) the effect of
as well as related disciplines (see Appendix S1). distance from the mainland on immigration rate. Predicted species
Compared to the broad literature reviewing IBT and its leg- numbers appear on the x-axis, with dotted arrows marking equilibria
acy, surprisingly little has been written about the wider contri- between immigration and extinction rates.

Review and Synthesis Islands as model systems 3
Box 2 Glossary
Anagenetic species: a species confined to a region (e.g. island or archipelago) whose sister lineage occurs outside that region.
Cladogenetic species: a species confined to a region (e.g. island or archipelago) whose sister lineage is also confined to that
region.
De novo community assembly: assembly of a community of species in an area where they were all previously absent.
De novo island: an island devoid of life upon formation, e.g. emerging as a result of volcanism or falling water level.
Ecological neutrality: the chances of an individual’s reproduction and death are independent of its species identity.
Fragment island: an island formed by separation from another landmass or island, thereby bearing a biota upon formation, e.g.
formed by plate tectonics or rising water level.
In situ: occurring within the geographical region of interest.
provided by islands for future advances in ecology and evolu- et al. 2010). A repeated theme in several chapters of The
tion. Origin of Species is Darwin’s (1859) use of a variety of
islands around the world to illustrate how presences,
absences, affinities and patterns of species richness are at
Islands as model systems
odds with these views and particularly with the notion that
Islands have played a key role in evolutionary theory from species are immutable. Islands provided Darwin the insights
its inception; while the particular insights of Darwin regard- for his theory of descent from common ancestry, and from
ing the fauna of the Gal apagos Islands continue to receive distinct geographical source areas. Studies of island biotas
much attention, the broader use of islands as tools by both led Wallace (1855) to draw the same conclusions indepen-
Darwin and Wallace to establish the theory that was so dently of Darwin, and later to defend evolutionary theory
controversial in their time is less often noted. Prior to their (Wallace 1880).
work, the prevailing view was that species were immutable
If we look to the islands off the American shore, how-
and created independently. Differences in species assem-
ever much they may differ in geological structure, the
blages across the planet were largely explained by historical
inhabitants, though they may be all peculiar species, are
patterns of species spread from a special point (or points)
essentially American. We may look back to past ages
of creation and abiotic controls on distribution (Lomolino
Box 3 Connections between different insular systems

This article focuses on terrestrial islands surrounded by water that have arisen devoid of life (de novo; Box 2). However, many
other insular systems are also relevant to some of the points raised and may provide substantial opportunities for research.
From a biological perspective, a key characteristic that varies between insular systems is whether ‘islands’ (surrounded by water
or otherwise) have arisen de novo, or as a result of the fragmentation of an existing landmass or habitat (Box 2; Gillespie &
Roderick 2002). In de novo systems, species number rises following formation, as a result of the rate of colonisation exceeding
that of extinction (Box 1). By contrast, on fragment ‘islands’, species number is expected to fall following formation (Box 1),
because the rate of extinction should exceed that of colonisation (relaxation; Whittaker and Fernandez-Palacios 2007). Origins
aside, fragment islands surrounded by water can share many key attributes with the focal islands of this review (Table 1, col-
umn II).
Some lakes (especially those lacking connections to other lakes, e.g. by way of rivers) provide almost perfect analogues to
islands surrounded by water. However, apparent ‘de novo origins’ do not always carry the same implications, since even in the
absence of connecting rivers, many lakes are filled by watercourses. Such lakes are therefore not devoid of life upon formation,
even if species numbers increase following formation through colonisation exceeding extinction. Also, lake volume may be as
relevant as area in assessing ‘niche space’.
For terrestrial organisms on islands, even if they show varying abilities to cross the surrounding water and colonise other
landmasses, water itself cannot be colonised (i.e. land is needed to reproduce). The same is often not true for the myriad of
other insular systems (such as montane sky islands, caves, and fragmented landscapes or aquatic environments), since the inter-
vening matrix consists of habitat from which some species may be able to colonise an ‘island’. Furthermore, there may be tran-
sitory possibilities for organisms to inhabit the matrix (e.g. because some species, normally restricted to forest fragments, can
inhabit the surrounding grassland in years of exceptional rainfall). A consequence of both of these tendencies is that isolation
(and corresponding in situ evolutionary change and endemism) tends to be less pronounced per unit distance of surrounding
matrix in many insular systems than it is for islands surrounded by water (e.g. Gillespie & Clague 2009).

Box 4 Examples of classic insights from islands into the ecology and evolution of communities
Communities are often but not always formed from the closest source pools
MacArthur & Wilson (1963, 1967) formalised expectations about distance to source pools in biota assembly; a corollary of Core
IBT is that the largest proportion of island immigrants will come from the nearest mainland source. They also discussed numer-
ous factors that may cause the geographical affinities of communities to differ from this prediction. These include long-distance
dispersal events and a series of factors that can permute the effects of distance on dispersal such as the sizes of source and reci-
pient areas, and the existence of stepping-stone islands. Other factors include wind and ocean currents, modes of dispersal, the
elevation and topographic complexity of the landmasses concerned, and temporal dynamics of these variables (Whittaker and
Fernandez-Palacios 2007; Lomolino et al. 2010).
The simplicity of island systems in delimiting geographic areas has been exploited in numerous phylogenetic methods of his-
torical biogeography to infer the effects of distance and direction of source pools in biota assembly (Ronquist & Sanmartın
2011). They have thus made it possible to identify situations that both support and contradict predictions regarding elementary
models of dispersal and factors that permute the effect of distance. Examples conforming to predictions come from the Hawai-
ian Islands. Consistent with the direction of extreme storms, taxa with high aerial dispersal abilities have predominantly colon-
ised the archipelago from the east. By contrast, insects capable of rafting have predominantly colonised from the southwest,
consistent with the location of stepping-stone islands (Gillespie et al. 2012).
Cases that contradict predictions have frequently revealed unappreciated dispersal, and the conditions under which propagules
are able to establish new populations. For example, in the presence of stepping-stone islands between remote islands and main-
land source pools, some highly dispersive taxa (spiders and birds) appear to have colonised remote islands directly and indepen-
dently from mainland sources (Gillespie et al. 2008). Such patterns lend support to the hypothesis that for these taxa single
extreme long-distance dispersal events are more probable than the combined probability of consecutive shorter dispersal events
(Nathan 2006).
Evolution can play a key role in community assembly

The spatial and temporal scales over which trait evolution occurs are recurrently controversial. For example, in response to the
dramatic and frequent climatic shifts of the Quaternary, paleoecological data have long supported major continental-scale range
shifts. Although such studies imply repeated community assembly and disassembly at timescales of 10 000–100 000 years, phe-
notypic change in response to such events is notably scarce (Bennett 1997). As a result of their isolated and replicated nature,
islands have long been used to illustrate the existence of in situ evolutionary change in biota assembly. Evolutionary change fol-
lowing colonisation was originally inferred from the wealth of endemic species in island settings (Darwin 1859), and a mass of
molecular data has since substantiated such inferences from morphology (Gillespie & Clague 2009). Further, numerous insular
evolutionary patterns indicative of changes in selective pressures following arrival on islands are documented (Grant 1998; Lo-
sos & Ricklefs 2009), and are variably attributed to changes in population size, the abiotic environment, and the newfound
presence or absence of particular other species (character displacement and character release, respectively).
In situ speciation is an important source of diversity

On continents, in the absence of a fossil record, the facility with which species distributions can change over time may easily
confound attempts to identify the precise geographical setting in which speciation has occurred. In combination with molecular
phylogenetic data, the isolation, discrete nature, and high levels of endemism on islands have been key in demonstrating that in
situ speciation can contribute significantly to biota assembly. Strong evidence for speciation having occurred within an island or
archipelago is provided by the monophyly of species endemic to that region. Accordingly, for example, it appears that 150 spe-
cies of diving beetle are the product of a single colonisation event followed by speciation within the island of New Guinea
(Balke et al. 2007), and 1000 species of picture-winged Drosophila are the product of speciation within the Hawaiian archipelago
(O’Grady et al. 2011). Islands have illustrated that the factors that interact to provide conditions necessary for in situ speciation
include isolation (Manceau et al. 2010), age (Gillespie & Baldwin 2010) and area (Losos & Schluter 2000; Kisel & Barraclough
2010) of the region concerned, and variables often associated with area, such as topographic complexity and elevation (Whittak-
er et al. 2008).
[. . .] and we find American types then prevalent on the out space and time, over the same areas of land and
American continent and in the American seas. We see in water, and independent of their physical conditions. The
these facts some deep organic bond, prevailing through- naturalist must feel little curiosity, who is not led to

Box 4 Examples of classic insights from islands into the ecology and evolution of communities
Communities are often but not always formed from the closest source pools
MacArthur & Wilson (1963, 1967) formalised expectations about distance to source pools in biota assembly; a corollary of Core
IBT is that the largest proportion of island immigrants will come from the nearest mainland source. They also discussed numer-
ous factors that may cause the geographical affinities of communities to differ from this prediction. These include long-distance
dispersal events and a series of factors that can permute the effects of distance on dispersal such as the sizes of source and reci-
pient areas, and the existence of stepping-stone islands. Other factors include wind and ocean currents, modes of dispersal, the
elevation and topographic complexity of the landmasses concerned, and temporal dynamics of these variables (Whittaker and
Fernandez-Palacios 2007; Lomolino et al. 2010).
The simplicity of island systems in delimiting geographic areas has been exploited in numerous phylogenetic methods of his-
torical biogeography to infer the effects of distance and direction of source pools in biota assembly (Ronquist & Sanmartın
2011). They have thus made it possible to identify situations that both support and contradict predictions regarding elementary
models of dispersal and factors that permute the effect of distance. Examples conforming to predictions come from the Hawai-
ian Islands. Consistent with the direction of extreme storms, taxa with high aerial dispersal abilities have predominantly colon-
ised the archipelago from the east. By contrast, insects capable of rafting have predominantly colonised from the southwest,
consistent with the location of stepping-stone islands (Gillespie et al. 2012).
Cases that contradict predictions have frequently revealed unappreciated dispersal, and the conditions under which propagules
are able to establish new populations. For example, in the presence of stepping-stone islands between remote islands and main-
land source pools, some highly dispersive taxa (spiders and birds) appear to have colonised remote islands directly and indepen-
dently from mainland sources (Gillespie et al. 2008). Such patterns lend support to the hypothesis that for these taxa single
extreme long-distance dispersal events are more probable than the combined probability of consecutive shorter dispersal events
(Nathan 2006).
Evolution can play a key role in community assembly

The spatial and temporal scales over which trait evolution occurs are recurrently controversial. For example, in response to the
dramatic and frequent climatic shifts of the Quaternary, paleoecological data have long supported major continental-scale range
shifts. Although such studies imply repeated community assembly and disassembly at timescales of 10 000–100 000 years, phe-
notypic change in response to such events is notably scarce (Bennett 1997). As a result of their isolated and replicated nature,
islands have long been used to illustrate the existence of in situ evolutionary change in biota assembly. Evolutionary change fol-
lowing colonisation was originally inferred from the wealth of endemic species in island settings (Darwin 1859), and a mass of
molecular data has since substantiated such inferences from morphology (Gillespie & Clague 2009). Further, numerous insular
evolutionary patterns indicative of changes in selective pressures following arrival on islands are documented (Grant 1998; Lo-
sos & Ricklefs 2009), and are variably attributed to changes in population size, the abiotic environment, and the newfound
presence or absence of particular other species (character displacement and character release, respectively).
In situ speciation is an important source of diversity

On continents, in the absence of a fossil record, the facility with which species distributions can change over time may easily
confound attempts to identify the precise geographical setting in which speciation has occurred. In combination with molecular
phylogenetic data, the isolation, discrete nature, and high levels of endemism on islands have been key in demonstrating that in
situ speciation can contribute significantly to biota assembly. Strong evidence for speciation having occurred within an island or
archipelago is provided by the monophyly of species endemic to that region. Accordingly, for example, it appears that 150 spe-
cies of diving beetle are the product of a single colonisation event followed by speciation within the island of New Guinea
(Balke et al. 2007), and 1000 species of picture-winged Drosophila are the product of speciation within the Hawaiian archipelago
(O’Grady et al. 2011). Islands have illustrated that the factors that interact to provide conditions necessary for in situ speciation
include isolation (Manceau et al. 2010), age (Gillespie & Baldwin 2010) and area (Losos & Schluter 2000; Kisel & Barraclough
2010) of the region concerned, and variables often associated with area, such as topographic complexity and elevation (Whittak-
er et al. 2008).
[. . .] and we find American types then prevalent on the out space and time, over the same areas of land and
American continent and in the American seas. We see in water, and independent of their physical conditions. The
these facts some deep organic bond, prevailing through- naturalist must feel little curiosity, who is not led to

Table 1. (continued)
Why islands?
(II) Key attributes used
Hard Replicated High De novo Small Climatic Known (III) Employment of key
6 B. H. Warren et al.
(I) Research Questions boundaries Isolation nature endemism origin size stability age attributes (IV) Promising approaches and study systems
inferring low vs. high spiders & Drosophila fruiflies, Canarian

potential for gene flow Tarphius beetles.
independent of genetic
data.

Can gene flow promote As above. Approach: As above. A role in speciation for
speciation? If so, how? phenomena associated with gene flow (e.g.
increased genetic and phenotypic variance,
reinforcement, coupling or immediate
reproductive isolation) should meet two
criteria: (1) occur in recently diverged species
pairs, not just in more deeply diverged (post-
speciation) pairs; (2) be absent from
inter-island species pairs, or at least
significantly less prevalent than for intra-island
pairs.
Study systems: As above.
Patterns of species richness
Why are some lineages (1) High incidence of Approach: For species-rich vs. species-poor
more diverse than endemic lineages with clades in a common island or archipelago
others? identical distributions, setting, coupling of:
(2) High incidence of (1) macroevolutionary phylogenetic studies to
intraspecific divergence disentangle factors such as time and net rate
occurring in the same of diversification in explaining differences in
context (geographic, species richness,
ecological) as (2) population genomic studies of co-
interspecific distributed species from within different clades,
diversification occurred. in which intraspecific divergence is occurring
in the same context (geographic or ecological)
as interspecific diversification has occurred.
Widespread (multiple-island) members of
insular clades otherwise composed of many
single-island endemic species may be
particularly good candidates. Comparisons can
be made between different lineages along
estimated time series following arrival.
Coupling of (1) and (2) provides potential to
examine the role of factors such as selection
and gene flow in underlying differences in
diversification rate.
What are the relative (1) Facility of inferring Approach: Extension of existing models (e.g.
contributions of barriers to gene flow, McPeek 2008; Pigot et al. 2010; Aguilee et al.
different modes of and temporal dynamics 2013) to predict how variation in mode of
speciation (e.g. of these barriers. (2) speciation affects components relating to
(continued)
Review and Synthesis
Why islands?
geographical, Replicates of different species-richness patterns (e.g. shape of

ecological) in driving temporal dynamic phylogenies, ecological trait distributions).
patterns of species- histories of barriers to Study systems: Archipelagos suitable for
richness? gene flow. testing predictions should have a variable (and
reconstructed) history of barriers to gene flow,
and in-depth data relating to species-richness
(phylogeny, and ecological traits) across
multiple island clades to compare with the
models (e.g. the Macaronesian archipelago).
What are the roles of (1) Facility of inferring Approaches:
equilibrium vs. non- immigration, extinction (1) Using ‘geographic’ lineage-based models to
equilibrium dynamics (both local and total), compare scenarios of unbounded (constant
in governing observed and that speciation has diversification rates) and bounded (declining
patterns of species occurred in situ. (2) diversification rates) diversity to a wider range
richness? ‘‘Clean slates’’ for of taxonomic and island systems (Rabosky &
studying community Glor 2010).
assembly. (2) Extending current ‘global scale’ lineage-
based models that were explicitly designed to
test for equilibrium dynamics (Morlon et al.
2010) to give them a spatial structure and
apply them to island systems.
(3) Studying spatially-explicit individual-based
models in their transient dynamics (including
responses to perturbation, e.g. mass extinction)
and developing phylogenetic inference tools
that can be used to fit these models to
phylogenetic data on islands.
(4) Analysing the distinct signature that
transient vs. equilibrium dynamics arising from
individual-based models may leave on
ecological (immigration – local extinction
dynamics, species abundance distributions,
species area relationships, distance-decay
relationships) and macroevolutionary
(phylogenies) island patterns.
(5) Fitting stochastic models incorporating
immigration, speciation and extinction
(Valente et al. 2014) to phylogenetic data from
communities on islands to test whether the
whole community or specific clades are
governed by equilibrium dynamics or are
fundamentally non-equilibrial.
Islands as model systems 7

Why islands?
6 B. H. Warren et al.
inferring low vs. high spiders & Drosophila fruiflies, Canarian

potential for gene flow Tarphius beetles.
independent of genetic
data.

Can gene flow promote As above. Approach: As above. A role in speciation for
speciation? If so, how? phenomena associated with gene flow (e.g.
increased genetic and phenotypic variance,
reinforcement, coupling or immediate
reproductive isolation) should meet two
criteria: (1) occur in recently diverged species
pairs, not just in more deeply diverged (post-
speciation) pairs; (2) be absent from
inter-island species pairs, or at least
significantly less prevalent than for intra-island
pairs.
Study systems: As above.
Patterns of species richness
Why are some lineages (1) High incidence of Approach: For species-rich vs. species-poor
more diverse than endemic lineages with clades in a common island or archipelago
others? identical distributions, setting, coupling of:
(2) High incidence of (1) macroevolutionary phylogenetic studies to
intraspecific divergence disentangle factors such as time and net rate
occurring in the same of diversification in explaining differences in
context (geographic, species richness,
ecological) as (2) population genomic studies of co-
interspecific distributed species from within different clades,
diversification occurred. in which intraspecific divergence is occurring
in the same context (geographic or ecological)
as interspecific diversification has occurred.
Widespread (multiple-island) members of
insular clades otherwise composed of many
single-island endemic species may be
particularly good candidates. Comparisons can
be made between different lineages along
estimated time series following arrival.
Coupling of (1) and (2) provides potential to
examine the role of factors such as selection
and gene flow in underlying differences in
diversification rate.
What are the relative (1) Facility of inferring Approach: Extension of existing models (e.g.
contributions of barriers to gene flow, McPeek 2008; Pigot et al. 2010; Aguilee et al.
different modes of and temporal dynamics 2013) to predict how variation in mode of
speciation (e.g. of these barriers. (2) speciation affects components relating to
(continued)
of the 1967 monograph MacArthur and Wilson expanded opportunities to vary arrival history in a predictable and repli-
their scope to consider the identity and ecology of species cated manner. Such ‘experiments’ have more confounding fac-
capable of forming a community. Diamond (1975) also had tors than microcosm experiments in which important
this perspective in elaborating a set of assembly rules govern- variables such as the traits of organisms are easily controlled,
ing island species composition. Though much controversy has but have the advantage of being natural, and including higher
ensued (see Whittaker and Fernandez-Palacios 2007; Simberl- organisms. First, little is known about how arrival interval
off & Collins 2010), the important message is that, as result influences ecological networks and the outcome of community
of their discrete and replicated nature, islands provide excel- assembly; in a microcosm experiment, the spacing of arrivals
lent settings in which to make predictions about community had a strong influence, as a result of competition and indirect
assembly, in particular how different lineages respond and facilitation (Fukami et al. 2007). These intervals are easily
interact during the process. Here we look at prospects of manipulated in island settings, arrivals being more closely
island-based approaches to refine predictions about how com- spaced on near islands than far ones. Second, an untested
munities form. hypothesis is that stochastic variability in arrival sequence
increases with distance from the source (Thornton 1996). Rep-
The role of arrival history in the assembly of ecological licates of de novo or sterilised islands both near and far from
networks a mainland source (Table 1) would provide the opportunity to
Since Core IBT (Box 1) does not consider species identity, the test this hypothesis, and evaluate the consequences of arrival
sequence of immigration is effectively random. The problem is history on ecological networks and the outcome of commu-
that the process of building up a network of ecological inter- nity assembly. Species compositions should be more variable
actions is poorly known; both this process and resulting spe- among islands in which stochastic variability of arrival is
cies compositions may be greatly influenced by the order and high, than among those in which its effect is lower. However,
timing of arrivals, and by the ecological characteristics of the precise relationship between variability of arrival and spe-
both newly arriving and established taxa (e.g. Fukami et al. cies composition may be complex; strong ecological interac-
2010). Arrival history is particularly relevant when feedback tions and feedbacks could amplify stochastic variability, while
loops reinforce ecological interactions. Important insights facultative changes in a species’ ecological position (e.g. diet,
regarding the role of interaction networks in community see Terborgh 2010) could have dampening effects. Such
assembly have come from two island systems; Krakatau and empirical studies, that effectively manipulate arrival history
mangrove islands in the Florida Keys. Repopulation of the within natural systems, have great potential to refine our
Krakatau islands following the violent eruption in 1883 understanding of the roles of arrival history vs. ecological net-
showed that the final outcome in terms of species composition works in driving deterministic sequences and outcomes of
could not be entirely predicted, reflecting in part historical community assembly.
contingency and stochastic components of colonisation
sequence and associated cross-trophic level linkages (reviewed How and why species abundances change during community
by Whittaker and Fernandez-Palacios 2007). The repopulation assembly
of Simberloff & Wilson’s (1971) artificially defaunated man- Ecological communities can be characterised not only by the
grove islands in the Florida Keys demonstrated shifts in tro- number of species they support, but also by the relative abun-
phic structure over time, and that the proportion of specialist dances of those species. Although continual changes in species
species increased during food-web assembly relative to gener- abundance are implicit both in de novo community assembly
alist species (Piechnik et al. 2008). (Box 2) and dynamic equilibrium, few theories address these
The availability of such empirical data from islands has dynamics. Given that Core IBT (Box 1) does not consider
recently made it possible to test an extension to Core IBT. species identities or population sizes, a logical extension of
While retaining the simplicity of Core IBT in modelling com- that theory is to consider how abundance distributions across
plex phenomena with few parameters, Gravel et al. (2011) species, and the abundance of individual species, change fol-
have shown how species interactions could easily be incorpo- lowing colonisation of an island by founding individuals. An
rated with important consequences for the shape of the spe- appropriate null hypothesis for population change is the
cies-area relationship and even for the number of trophic assumption of ecological neutrality (Hubbell 2001). Such an
levels expected in fragmented systems. Realistic network struc- approach has been taken by extending individual-based eco-
tures and assembly sequences are predicted simply by assum- logical neutral theory (Hubbell 2001) to predict species abun-
ing a sequential and conditional assembly process (e.g. a dance distributions on islands over timescales that cover
predator/pollinator requiring at least one prey/plant to estab- immigration, extinction, and in situ evolution (Rosindell &
lish and persist). Thus, accounting for species identity in IBT Phillimore 2011), and with reference to the approach to and
provides a powerful framework to investigate the reciprocal attainment of dynamic equilibrium (Rosindell & Harmon
feedbacks between assembly dynamics and community struc- 2013). Clearly, however, factors such as ecological release,
ture (Gravel et al. 2011, and references therein). unequal competitive abilities, predation, parasitism, and
Notwithstanding this advance, there is still much to learn changes in environmental conditions, are expected to influence
about how arrival history influences the build-up of ecological abundance dynamics in very non-neutral ways. For example,
interactions and resulting species compositions. Small de novo the taxon cycle describes a pattern in which lineages go
or sterilised islands that differ in their isolation from the through sequential phases of expansion and contraction dur-
mainland (see Table 1 for examples) provide important ing the assembly of an insular community (MacArthur &

Wilson 1967; Ricklefs & Bermingham 2002, and references increase with island isolation. Integrating ecological neutral
therein). It has been suggested that expansion is driven by theory into island biogeography, Rosindell & Phillimore
ecological release from predation or disease in a new environ- (2011) recently made more precise predictions regarding the
ment, and that subsequent decline is the result of ‘counterad- location of zones of anagenesis and cladogenesis at equilib-
aptation’ of insular enemy species (Ricklefs & Bermingham rium, with respect to island isolation and area. Cladogenetic
2002, and references therein). Carlquist (1966) also highlighted species (Box 2) are predicted to occur above thresholds in
a loss of competitive ability in island lineages, as one of his 24 both island area and isolation, and in greater numbers on the
principles of dispersal and evolution. He posited loss of largest and most distant islands. Anagenetic species richness
genetic variability or evolutionary specialisation as potential (Box 2) is also predicted to increase with island area, but to
causes, although he lacked a comprehensive explanation for peak on islands of intermediate isolation.
the latter. Specialisation to local environments might increase This humped distribution of anagenetic species with dis-
fitness on the generational timescale upon which selection tance results from a trade-off: immigration must be small
acts, but reduce tolerance to changes arising over longer time- enough to escape the homogenising effects of gene flow with
scales, such as new arrivals and major environmental change, the mainland population that prevent divergence (Johnson
as well as reducing evolutionary lability in response to such et al. 2000), but also frequent enough to initiate anagenesis
events. repeatedly and keep temporal turnover high enough to pre-
Knowing how species abundances change over timescales vent anagenetic species from persisting for long enough to
encompassing both evolutionary change and in situ speciation radiate and become cladogenetic. Consistent with these pre-
would aid our understanding of community assembly, but dictions, support has been obtained for a model in which
such information is difficult to obtain. Nonetheless, barring highest species richness occurs among lineages of intermediate
extinction and back-colonisation (see Appendix S2), the ages dispersal ability, such that dispersal is sufficiently frequent to
of endemic populations on de novo islands can be inferred allow repeated colonisation across geographic barriers, but
from genetic distances to their source populations on the sufficiently limited to restrict gene flow across these barriers
mainland or other islands. Testing predictions for the relation- (Claramunt et al. 2012; Agnarsson et al. 2014). However, this
ship between species abundance and age using a neutral model assumes that a lineage’s dispersal ability remains con-
model (Rosindell & Phillimore 2011), including predictions stant through time. In reality, many cases of reduced dispersal
concerning the approach to dynamic equilibrium as well as ability following island colonisation are known, both in ani-
population behaviour at equilibrium, would be informative mals and plants, and are principally attributed to changes in
about the processes underlying species abundance distribu- selective regimes following island colonisation (Carlquist 1966;
tions. Failure to reject such a model would imply a key role Grant 1998). Such insular changes are known to influence the
for dispersal and available space on an island in explaining spatial scale at which population differentiation occurs (Blon-
abundance dynamics, while deviation from its predictions del et al. 1999). Thus, any generalisation on how dispersal
would implicate other ecological processes. For example, ability influences island species richness remains provisional,
under ecologically neutral models, high abundance is achieved and future studies might compare focal lineages of high dis-
via the slow process of drift and therefore the highest abun- persal ability that readily lose this ability (e.g. birds) with
dance class would be predominantly occupied by old species, those that do so rarely (e.g. mosses and ferns).
while under ecological release abundant species should be pre- An additional explanation for isolation promoting anagene-
dominantly recent arrivals. If competition or predation were sis is that under a low rate of colonisation populations are
involved in the decline of an island population from the high- exposed to less competition, which gives them more time to
est abundance class, the mean time to extinction would be differentiate anagenetically before they are displaced (Price
shorter than under the ecologically neutral model (Ricklefs 2008; Rosindell & Phillimore 2011). However, these factors
2006). Studies of the species age-abundance relationship on work in the opposite direction to the ‘rescue effect’, in which
islands testing predictions of alternative models should pro- at low isolation the more frequent arrival of propagules pro-
vide insight into the role of ecological differences between spe- tects island populations from extinction through the demo-
cies in moulding species abundance distributions. graphic and genetic contributions of later immigrants (Brown
& Kodric-Brown 1977).
How evolution may influence community assembly: predicting A low rate of colonisation of remote islands also tends to
the effects of geographic area and isolation promote cladogenesis by leaving niches ‘open’ for long peri-
While evolution and speciation were absent from Core IBT ods, allowing them to be filled as readily by in situ speciation
(Box 1), MacArthur & Wilson (1963) included a term for spe- as by dispersal (Gillespie & Baldwin 2010). Intuitively, island
ciation by in situ cladogenesis in the first mathematical state- area may also affect the potential for species diversification
ment of the equilibrium model. They left out speciation by both by increasing opportunities for intra-island allopatry and
anagenetic change as their focus at this point was on the by adaptation to more diverse habitats that can be accommo-
establishment of equilibrium species numbers, which is dated on larger islands (Losos & Schluter 2000). Furthermore,
unchanged by anagenesis. They also explicitly recognised the larger areas imply larger population sizes, likely increasing
important role of speciation in contributing to species richness both the number of advantageous mutations and the efficiency
within sufficiently isolated archipelagos, in what they termed with which selection acts upon them (Gavrilets & Losos
the ‘radiation zone’. They thus recognised within their theory 2009). Several island-based studies have confirmed the impor-
that the contribution of speciation to species richness would tance of area in cladogenesis (Losos & Schluter 2000; Kisel &

Barraclough 2010; Rabosky & Glor 2010). However, beyond absence of in situ evolutionary change, by a process that he
Rosindell & Phillimore’s (2011) test of their own predictions termed ‘ecological fitting’: a combination of immigration,
with island bird data, how the interplay between isolation and environmental filtering and species interactions. His hypothe-
area influences the relative importance of anagenesis and clad- sis stemmed from observation that the majority of species rep-
ogenesis largely remains to be evaluated (but see Johnson resented have vast distributions across the Americas, and little
et al. 2000; Valente et al. 2014). Islands provide key settings phenotypic variability between sites.
for such future empirical and theoretical study of biota assem- Beyond an understanding of the importance of different
bly. processes in community assembly, a useful future direction is
to understand how assembly processes influence ecosystem
functioning (Venail et al. 2008; Fukami et al. 2010). In situ
Ecosystem functioning
evolution might influence ecosystem functioning as a result of
With the prospect of human activities leading to a global eco- both adaptation of individual species to the local environment
logical crisis, Loreau (2010) has called for the unification of and coevolution of two or more component species (Schoener
population, community, ecosystem and evolutionary ecology 2011). Does in situ evolution therefore contribute to ecosystem
into a single discipline of evolutionary ecosystem ecology. productivity, efficiency or other properties, and to what
One of the greatest challenges in this integration was identi- degree? This question has strong implications for society in
fied as the gap between evolutionary biology, which seeks predicting and mitigating the impacts of human-induced glo-
principles at the levels of genes, individuals and populations, bal change. While some landmark studies have recently
and ecosystem ecology, which seeks principles at the higher approached the problem using microbial systems (see e.g. Ve-
organisational level of the ecosystem (Loreau 2010). We nail et al. 2008), islands, as a result of their isolation and rep-
believe that islands provide excellent systems to explore licated nature, may be excellent model systems with which to
whether coupling evolutionary and ecosystem dynamics can investigate such issues with higher organisms. Archipelagos
lead towards a better understanding of the processes shaping containing many small (ca. 1–100 km2) islands can provide
ecosystems. First, the small size and isolation of islands has replicates of two different situations, in which the physical
long made them systems of choice for illuminating the role of environment (climate, geology and topography) is similar both
species interactions on ecosystem functioning (for a recent within and among islands, or nearly so: (1) islands supporting
example, see Fukami et al. 2006). Second, the very high pro- native habitat in which human influence is minimal, and many
portion of endemic lineages (subspecies, species, and higher taxa are endemic and (2) islands in which human influence
orders) on islands makes for communities in which the contri- has been dramatic, and much of the biota is introduced, with
bution of in situ evolution to community assembly is both little native habitat and fewer endemic taxa remaining. The
large and relatively easily identified (e.g. Gillespie 2004; Clegg presence of single-island endemic species or subspecies would
2010). suggest a substantial role for in situ evolution in the assembly
of the former community, while it would be negligible or
Determining the relative roles of in situ evolution and ecological absent from the latter. An example of an archipelago that
fitting in ecosystem functioning could meet these conditions is the Aldabra Group (Box 5 case
Despite the high incidence of readily detectable in situ adap- study).
tive evolutionary change in the assembly of insular biotas, its To examine the contribution of in situ evolution to ecosys-
importance at a small (community) scale within continents tem functioning, suitable measures for comparison between
has been questioned. Janzen (1985) proposed that a Costa islands may include net primary production, various measures
Rican forest community is principally assembled in the based on nutrient cycling, and measures based on plant–soil
Box 5 A case study archipelago for inferring the relative role of in situ evolution and ecological fitting in ecosystem functioning: the Aldab-
ra Group of the western Indian Ocean
The Aldabra Group of the Seychelles in the western Indian Ocean may present a suitable example of an archipelago with the
features needed to understand the relative contribution of ecological fitting (Box 6) and in situ evolution in ecosystem function-
ing. The approach compares (1) a community in which the majority of lineages have undergone in situ evolution following their
arrival and (2) a community created by ecological fitting of species that have evolved elsewhere. Within the Aldabra Group, the
former situation occurs on the islands of Aldabra Atoll (UNESCO World Heritage Site), which are among the least disturbed
of all low latitude islands, with many endemic species (Stoddart & Wright 1967). By contrast, the neighbouring islands of
Assumption, Cosmoledo and Astove frequently present the latter situation. Although once similar to the islands of Aldabra
Atoll, they have been extensively transformed by human activity. In particular, the mixed scrub community of Assumption is
composed of many introduced plant species, despite being similar in overall species richness to that of Aldabra Atoll (Stoddart
et al. 1970). Such islands are also very similar to those of Aldabra Atoll in size, topography and climate, and therefore present
informative points of comparison.

(a) Speciation strictly allopatric (b) Speciation with gene flow
Gene 1 Gene 2 Gene 3 Gene 1 Gene 2 Gene 3
Figure 2 Predictions regarding genomic signatures of different speciation modes after Bachtrog et al. (2006). t, time since divergence; TMRCA, time since
most recent common ancestor. (a) speciation strictly allopatric, no difference in t between loci; (b) speciation with gene flow, t differs.
feedbacks (Vitousek 2004; Bardgett & Wardle 2010). Within from closely related species. They argued that under strict
this framework, linking the diversity of decomposers and of allopatry (i.e., no gene flow), all regions of the genome will
decomposition rates appears to be a particularly promising have a single divergence history, and vary only in their coales-
avenue to investigate (see Ehrenfeld 2003). Clearly, ability to cence times (Fig. 2a). By contrast, in geographical contexts
eliminate confounding variables is key to the strength of an allowing gene flow (e.g. sympatry, parapatry, and when popu-
island-based test. Notably, species richness may vary between lations are separated but sufficiently close to allow regular dis-
islands and is known to influence ecosystem functioning persal between them), species may share regions that have not
(Hooper et al. 2005; Bardgett & Wardle 2010). Although dif- yet diverged functionally, or that function sufficiently well in
ferences in species number between islands resulting from in the recipient species as to be maintained by selection. As a
situ cladogenesis are a true reflection of in situ evolution, result, in the presence of gene flow, they predicted that the
those resulting from immigration are not. As a starting point genome will be a mosaic of different regions with disparate
for approximation, the number of immigration events contrib- divergence times (Fig. 2b). To the best of our knowledge,
uting to an island community can often be inferred from tax- these predictions remain to be explicitly tested using indepen-
onomy, and comparisons are possible between islands in dent (non-genetic) inferences regarding the geographic context
which they are constant, or nearly so. Going a step further, of divergence.
with increasing availability of molecular phylogenetic data Islands provide ideal systems to test these predictions
and advances in analytical interpretation, it is becoming possi- because of the frequent replication of two geographic
ble to quantify immigration with ever-increasing accuracy extremes within the same island radiation. First, such radia-
(e.g. Ronquist & Sanmartın 2011; Cornuault et al. 2013). tions frequently include sister-species pairs in which each
member of the pair is endemic to a different island, and in
which the two islands have never been connected. Such pairs
Geography, gene flow, and species diversification
provide cases for divergence in full allopatry, in which oppor-
Island systems have proven key in studying the process of tunities for gene flow are minimal when inter-island distance
population differentiation, as a result of being discrete, geo- exceeds the organism’s regular dispersal ability. Second, some
graphically isolated, replicated, and small in size relative to such radiations also contain sympatric or closely occurring
continents (e.g. Grant & Grant 2008). We illustrate how this sister species endemic to the same island (e.g. Hawaiian
situation provides underappreciated potential for investigating Tetragnatha and Drosophila: Gillespie & Baldwin 2010;
what are currently important topics in the biology of specia- O’Grady et al. 2011). These have high potential to have
tion, i.e. how divergence-with-gene flow may lead to specia- diverged in the presence of intermittent or ongoing gene flow.
tion, and distinguishing the effects of geography and ecology Under these conditions, same-island vs. different-island species
on genomic divergence and speciation (Feder et al. 2013; pairs offer a promising investigative framework. Coalescent
Seehausen et al. 2014). With respect to intraspecific diver- analyses (Sousa & Hey 2013) of multiple species pairs from
gence, the substantial environmental heterogeneity of many the same island radiation within such a framework would pro-
islands provides suitable settings for examining how different vide the data to test whether the alternatives proposed by
lineages respond to common environmental and geographical Bachtrog et al. (2006) correctly depict genomic patterns of
variation. We illustrate how this feature can aid in under- divergence in nature. If the alternatives are supported, such
standing why some lineages are more diverse than others. results may offer a baseline to infer levels of gene flow during
Although these prospects are the furthest removed from Core speciation, in cases where past biogeography (geographic
IBT, we believe that by addressing problems in a rapidly mov- proximity of lineages) is highly uncertain. Such comparisons
ing field, they present the most immediate potential for should also provide a test of the role of gene flow in shaping
advances using islands as model systems. patterns of divergence across the genome (Feder et al. 2013).
Determining the genomic signature of speciation with and Assessing the role of gene flow in speciation
without gene flow Beyond characterisation of how gene flow shapes patterns of
In an insightful paper, Bachtrog et al. (2006) proposed that genomic divergence, its consequences in promoting or retard-
different levels of gene flow during speciation can be distin- ing speciation can be expected to vary greatly between taxa,
guished using genealogical analysis of multilocus datasets stages of divergence, and spatial contexts (Abbott et al. 2013).

Three main mechanisms by which gene flow may promote diversity increases unbounded through time, and to distin-
speciation have been proposed. First, it can increase the guish between two alternative explanations for diversity varia-
genetic variance upon which selection can act (Smadja & But- tion among clades: differences in the time available for
lin 2011), potentially serving as a multilocus macromutation diversification, and differences in net diversification rate. Stud-
(Mallet 2007, and references therein), which may expand the ies using dated phylogenies have variably supported both
range of phenotypic variance on which natural selection can explanations (e.g. Rabosky et al. 2007; Cornuault et al. 2013).
act. Second, counterintuitively, it can promote reproductive A second step involves considering alternative explanations
isolation, by increasing the potential for reinforcement (Smad- for diversity dynamics such as diversity-dependence and
ja & Butlin 2011; Abbott et al. 2013) or by coupling genetic bounded diversity, equilibrium dynamics and periods of diver-
incompatibilities with ecological loci under disruptive selection sity decline (Morlon 2014, and references therein). The co-dis-
(Seehausen 2013). Third, it can create new species directly in tribution of both diversified and non-diversified lineages
the form of reproductively isolated hybrids (Abbott et al. across the same island or archipelago offers researchers some
2013). Clearly, however, the efficacy of the first two mecha- degree of control over the time, geographical area and envi-
nisms must also depend on conditions under which the ho- ronmental heterogeneity available for diversification. It also
mogenising effects of gene flow are overcome. Due to such offers some control over the environmental changes experi-
difficulties, the predominant impact of hybridisation on speci- enced by clades during their evolutionary history. Such set-
ation remains controversial (Barton 2013; Servedio et al. tings seem ideal to identify fundamental differences in the way
2013). species from diversified lineages respond to heterogeneity and
Empirical data shedding light on the genome-wide build-up temporal variation in environment and geography, compared
of barriers to gene flow are growing rapidly, via genome scans to species belonging to lineages that have not diversified.
and association mapping using large sets of individuals from Phylogenetic analyses chart the histories of species over deep
diverging lineages. This includes transects across hybrid zones, timescales, revealing, for example, differences in diversification
replicated combinations of lineages at different locations, and rates among lineages. The integration of population-level stud-
the comparison of closely related populations and species with ies with such higher order phylogenetic studies may provide
different divergence times (Abbott et al. 2013). However, as greater opportunity to connect phylogenetic pattern with evolu-
emphasised by Butlin & Ritchie (2009), the new plethora of tionary and ecological process. In a recent review, Losos &
genomic data will not clarify the genetics of speciation unless Ricklefs (2009) suggest that detailed population-level studies
it is possible to distinguish changes that have contributed to can chart the course of evolution over short time periods,
divergence and reproductive isolation from those that are car- directly measuring the extent to which natural selection changes
ried along in its wake. in strength and direction over time. This approach can be
Island radiations such as those proposed above, with both broadened to incorporate intraspecific-level studies with geo-
inter-island and intra-island sister-species pairs, would provide graphically explicit sampling of individuals for the reconstruc-
an ideal framework to address these issues. A further advan- tion of gene genealogies to reveal the extent to which natural
tage would be afforded by the presence of both inter-island selection, or alternative mechanisms (e.g. differences in neutral
and intra-island pairs that differ significantly in their degree divergence resulting from differences in dispersal ability; Ag-
of divergence, ranging from incipient species to species that narsson et al. 2014), may explain evolutionary change. Island
exhibit complete or nearly complete reproductive isolation. In radiations are ideal systems for such an approach, because it is
such a comparative framework, a role in speciation for phe- frequently apparent that the arena within which interspecific
nomena associated with gene flow (e.g. increased genetic and diversification has occurred is similar to the arena within which
phenotypic variance, reinforcement, coupling, or immediate intraspecific diversification is occurring (e.g. Ricklefs & Ber-
reproductive isolation) should meet two criteria. First, these mingham 2002). This likely results from the hard boundaries,
phenomena should be observed in recently diverged species isolation and climatic stability of islands (Table 1), despite geo-
pairs, not just in older (post-speciation) pairs. Second, they logical dynamics (Whittaker et al. 2008). Population genomic
should be absent from inter-island species pairs, or at least comparisons of lineages from species-rich and species-poor
significantly less prevalent than for intra-island pairs. clades in the same island or archipelago setting provide real
potential to determine the relative roles of factors such as the
Understanding why some lineages are more diverse than others strength of selection and gene flow in rendering one lineage
The proliferation of life on islands has progressed much far- more species-rich than another.
ther within some lineages than others. For example, among
the 88 native genera of weevils (Coleoptera, Curculionidae)
HOPES FOR THE FUTURE OF ISLAND-BASED THEORY
occurring naturally within the Canary Islands, there is an
average of only three species per genus (Whittaker and For many, MacArthur & Wilson’s (1963) model is the fore-
Fernandez-Palacios 2007, and references therein). However, most example of using islands as model systems. It can be
128 species, more than one-third of all the native weevil spe- seen as the founding core of a theory that has been and con-
cies in the Canary Islands, belong to a single genus, Laparoce- tinues to be greatly extended, providing a quantitative base-
rus (A. Machado, pers. comm.). Such island-based patterns line against which deviation can be tested. As such it has not
raise an important and more general question – why have just improved our understanding of island communities, but
some lineages diversified so extensively, while others have not? also brought important insights in ecology, evolution, bioge-
A first step in responding to this question is to assume that ography and community assembly in general (e.g. Hubbell

Box 6 Equilibrium vs. non-equilibrium, and the potential nature of equilibria

MacArthur and Wilson’s IBT explains species richness on an island from a dynamic balance between colonisation and extinc-
tion events (Box 1). While the theory has been greatly expanded (e.g. Brown & Kodric-Brown 1977; Hubbell 2001; Hanski
2010; Gravel et al. 2011; Rosindell & Phillimore 2011), the hypothesis of equilibrium dynamics is rarely brought into question
(but see Simberloff 1976, 1983; Gilbert 1980; Steadman 2006; Whittaker and Fernandez-Palacios 2007).
Two separate explanations for a lack of equilibrium are frequently confused, both on ecological and evolutionary timescales.
In one scenario, a biota is governed by processes that cause species richness to tend towards equilibrium, but this equilibrium
has not been reached, and in some cases may never be reached. We refer to this situation as unattained equilibrium. It may
occur when: (1) there has been insufficient time for the equilibrium in question to be reached. Examples include islands that are
young (be they de novo or fragment islands; Brown 1971), recently sterilised, large, or highly isolated; (2) there is a lag in the
response time of extinction, allowing equilibrium to be temporarily exceeded (Gillespie 2004; Gavrilets & Losos 2009); (3) envi-
ronmental fluctuations or disturbances outpace the time to equilibrium (McGuiness 1984; Whittaker 2000). In a second sce-
nario, species richness is simply not governed by equilibrium dynamics. We refer to this as fundamental non-equilibrium. For
example, on evolutionary (and potentially ecological) timescales, diversity may accumulate without limit (Emerson & Kolm
2005; Morlon et al. 2010), there being no a priori reason to believe that extinction should balance species accumulation.
A largely overlooked addition to IBT is E. O. Wilson’s (1969) hypothesis that equilibria can themselves shift during the
course of what is described today as community assembly (Fig. 3). He envisaged a time-progressive sequence in the relative
importance of the actions of species interactions (such as competitive exclusion), environmental filtering, adaptation, and co-
evolution during community assembly, leading to changes in the position of the equilibrium between immigration and extinc-
tion. Four equilibria were recognised on a hypothetical relative timescale:
(1) Non-interactive: an equilibrium reached prior to the attainment of sufficiently high population densities to make species
interference (including competitive exclusion) a major factor in extinction,
(2) Interactive: an equilibrium in which species interactions (including competitive exclusion) are a major factor in survivor-
ship,
(3) Assortative: an equilibrium occurring in response to environmental filtering, that is, the peculiar physical conditions of the
local environment and interactions with other species over the long term,
(4) Adaptive (to distinguish this from the equilibrium that follows, we avoid using Wilson’s term ‘evolutionary’): an equilibrium
reached when populations have had time to undergo evolutionary adaptive change in response to both local environmental con-
ditions and to other species. Such island populations may or may not be considered separate species from their continental rela-
tives.
The first three of these equilibria are based on empirical data from the Florida mangrove experiments that E. O. Wilson con-
ducted with D. Simberloff (Simberloff & Wilson 1971). In Fig. 3, we present a modified version of E. O. Wilson’s (1969)
schema, to which we have added a fifth equilibrium, more easily studied since the advent of molecular phylogenetics, in which
the effect of speciation (as well as immigration), offsets extinction:
(5) Radiative: an equilibrium occurring when lineages resulting from the adaptive phase have had time to undergo speciation
(cladogenesis) within the island or archipelago of interest.
E. O. Wilson (1969) considered his four equilibria as a time-progressive sequence, with evolutionary processes in the fourth
being clearly distinguished from ecological processes in the previous three. Today, evolutionary responses are widely recognised
to occur on timescales that are as short as ecological ones (Schoener 2011), and indeed natural selection will operate throughout
the five phases of equilibria. We therefore see the schema as a continuum, rather than a discrete sequence, and acknowledge
that at each phase, the processes leading to the previous equilibrium will still operate. Following Janzen (1985), we refer to the
process of environmental filtering and species interactions leading to the accommodation of extra species in the assortative equi-
librium as ‘ecological fitting’. We refer to the process of in situ adaptation, both to the environment and to other species, allow-
ing accommodation of extra species in the adaptive equilibrium as ‘evolutionary packing’.
2001; Hanski 2010; Losos & Ricklefs 2010). However, despite bility of non-equilibrium dynamics (both on ecological and
its success in predicting diversity patterns, over the 50 years evolutionary timescales) remains one of the greatest challenges
since its publication, the ability of IBT to identify underlying for the future (Box 6). We therefore advocate a judicious use
processes has received a range of critiques (Gilbert 1980; Wil- of island-based theory. This should include using the assets of
liamson 1989; Steadman 2006). In particular, the central pre- islands in allowing theories to be simple, but also remaining
mise of IBT – that of an equilibrium between immigration critical and continuing to question the core hypotheses and
and local extinction – remains equivocal and difficult to test assumptions involved. Here, we consider some hopes for the
(Simberloff 1976, 1983; Gilbert 1980). Incorporating the possi- future of island-based theory with these views in mind.

Figure 3 A schematic hypothesis for the time-progressive continuum of equilibria involved in community assembly (Box 6), modified from E. O. Wilson’s
(1969) Brookhaven paper. Following Wilson (1969), a hypothetical relative time scale is used. Equilibria between immigration and local extinction are
shaded red, while the equilibrium among immigration, speciation and local extinction is shaded purple. Once populations have differentiated in situ to the
species level, local extinction events will also be total extinction events.
and deceleration in the rate of lineage accumulation) can be

Modes of speciation
obtained purely from ecological speciation (McPeek 2008) as
In order to explain the spatial distribution of species diversity, well as purely from geographical speciation (Pigot et al.
in situ speciation needs to be taken into account. Accordingly, 2010). We therefore need new models to make quantitative
recent island-based models have incorporated speciation (e.g. predictions to assess the contribution of different modes of
Rosindell & Phillimore 2011). Ideally however, future island speciation in community assembly (Moen & Morlon 2014).
models should incorporate different modes of speciation, in These might include not only phylogenies, but also ecological
particular geographical speciation (for which geographical traits and species ranges. Such models provide the potential to
isolation is the component initiating genetic divergence) and more precisely predict the influence of area and temporal con-
ecological speciation (i.e. as a result of ecologically-based nectivity of available land on the spatial distribution of spe-
divergent selection). Further, many permutations of these sim- cies diversity.
plified scenarios are possible; different speciation events on
any one island may follow different modes, and any single
Understanding equilibrium vs. non-equilibrium dynamics
speciation event may result from a combination of different
modes, especially when geographical settings change during If species richness is to a large extent explained by non-equi-
speciation (Butlin et al. 2008). The latter may particularly librium dynamics (Box 6), non-equilibrium models and a bet-
apply when geological and environmental dynamics induce ter theoretical understanding of dynamics outside of
repetitive island connection and separation (Whittaker and equilibrium are still required (Whittaker and Fernandez-Pala-
Fernandez-Palacios 2007). Geographical isolation may thus cios 2007). For example, fundamental non-equilibrium models
contribute only intermittently to speciation. Likewise, progres- (see Box 6 for definition) could be achieved by integrating
sive phases of community assembly on islands (Box 6, Fig. 3) classic MacArthur & Wilson immigration–extinction processes
may alter the shape and strength of ecological selective pres- with time-variable macroevolutionary birth–death models of
sures that contribute to speciation. Variation in island size in situ diversification with no upper limits to diversity (Valente
(e.g. owing to sea level fluctuations) affects the overall proba- et al. 2014). This might be achieved with extinction rates that
bility of speciation (Losos & Schluter 2000; Kisel & Barrac- are constantly outstripped by the input of new species from
lough 2010) and may therefore also affect the contributing immigration and speciation, and so diversity grows without
mode(s) of speciation (Whittaker et al. 2008; Losos & Ricklefs bound. An alternative way to approach non-equilibrium the-
2009). Aguilee et al. (2013) recently developed a model allow- ory is simply to study the transient behaviour of models that
ing for such variable history, in which ecological speciation would in theory eventually equilibrate, but do not have the
includes temporary and repetitive geographical isolation. They opportunity due to lack of time or continuous environmental
show that temporal variation in geographic setting, inducing change (i.e. unattained equilibrium, Box 6; Ricklefs & Ber-
changes in the contribution of different speciation modes, is mingham 2001).
likely to facilitate speciation, possibly generating adaptive In the case of equilibrium models such as IBT, a better
radiation. In this context, models predicting biodiversity pat- understanding of the time it takes to reach equilibrium would
terns that can be compared to empirical data are, however, be useful. Perhaps the equilibrium towards which we are
still lacking. Realistic phylogenies (including tree imbalance heading is a moving target (e.g. Box 6, Fig. 3)? If so, in some

cases it may never be reached. To resolve these questions we tual framework and drafted sections of text, many of which
must study and model predictions over the time scales in were incorporated to a greater or lesser degree. BHW wrote
which equilibrium would be expected to be reached. This most of the manuscript, coordinated the ideas and input from
could include phylogenetic data, fossil data and ecological all co-authors and benefited throughout from substantial tech-
time series. In addition to studying the colonisation of newly nical and conceptual support and experience from all co-
formed or sterilised islands, changes in island characteristics authors. CT, DSi, BCE, RER and RGG provided substantial
(e.g. area, isolation, and topographic complexity) due to senior guidance regarding contents and format. RA, FLC,
ontogeny (Whittaker et al. 2008) or sea level change (Rijsdijk BCE, DG, HM, NM, JR and DSi contributed large blocks of
et al. 2014) provide underexploited situations in which to test time in writing and/or figure preparation. All authors read
whether equilibrium dynamics apply. and commented on drafts of the manuscript.
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Ecology Letters, (2014) doi: 10.1111/ele.

Ecology Letters (2014)

paper, ‘An equilibrium theory of insular zoogeography’, R.

© 2014 John Wiley & Sons Ltd/CNRS

(Simberloff 1976). On the other hand, MacArthur and Wil-

son’s broader aim – using islands as model systems to

© 2014 John Wiley & Sons Ltd/CNRS

Box 3 Connections between different insular systems

© 2014 John Wiley & Sons Ltd/CNRS

Evolution can play a key role in community assembly

In situ speciation is an important source of diversity

© 2014 John Wiley & Sons Ltd/CNRS

Evolution can play a key role in community assembly

In situ speciation is an important source of diversity

© 2014 John Wiley & Sons Ltd/CNRS

(II) Key attributes used

inferring low vs. high spiders & Drosophila fruiflies, Canarian

© 2014 John Wiley & Sons Ltd/CNRS

(II) Key attributes used

geographical, Replicates of different species-richness patterns (e.g. shape of

© 2014 John Wiley & Sons Ltd/CNRS

(II) Key attributes used

inferring low vs. high spiders & Drosophila fruiflies, Canarian

© 2014 John Wiley & Sons Ltd/CNRS

© 2014 John Wiley & Sons Ltd/CNRS

© 2014 John Wiley & Sons Ltd/CNRS

© 2014 John Wiley & Sons Ltd/CNRS

(a) Speciation strictly allopatric (b) Speciation with gene flow

Gene 1 Gene 2 Gene 3 Gene 1 Gene 2 Gene 3

© 2014 John Wiley & Sons Ltd/CNRS

© 2014 John Wiley & Sons Ltd/CNRS

Box 6 Equilibrium vs. non-equilibrium, and the potential nature of equilibria

© 2014 John Wiley & Sons Ltd/CNRS

and deceleration in the rate of lineage accumulation) can be

© 2014 John Wiley & Sons Ltd/CNRS

© 2014 John Wiley & Sons Ltd/CNRS

© 2014 John Wiley & Sons Ltd/CNRS

© 2014 John Wiley & Sons Ltd/CNRS

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