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Phylogenetic Insights on
Adaptive Radiation
Richard E. Glor
Department of Biology, University of Rochester, Rochester, New York 14627;
email: [email protected]
Annu. Rev. Ecol. Evol. Syst. 2010. 41:251–70
Key Words
First published online as a Review in Advance on
August 9, 2010
adaptation, phylogeny, diversification
The Annual Review of Ecology, Evolution, and
Systematics is online at ecolsys.annualreviews.org
Abstract
This article’s doi:
10.1146/annurev.ecolsys.39.110707.173447
c 2010 by Annual Reviews.
Copyright All rights reserved
1543-592X/10/1201-0251$20.00
Adaptive radiation is a response to natural selection and ecological opportunity involving diversification of species and associated adaptations. Although
evolutionary biologists have long speculated that adaptive radiation is responsible for most of life’s diversity, persistent confusion and disagreement
over some of its most fundamental questions have prevented it from assuming a central role in explaining the evolution of biological diversity. Today,
answers to many of these questions are emerging from a new wave of integrative research that combines phylogenetic trees with a variety of other data
and perspectives. In this review, I discuss how modern phylogenetic analyses
are central to (a) defining and diagnosing adaptive radiation, (b) identifying
the factors underlying the occurrence and scope of adaptive radiation,
(c) diagnosing predictable patterns of ecological diversification during
adaptive radiation, and (d ) reconstructing the history of adaptive radiations.
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INTRODUCTION
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Darwin’s finches, African Rift Lake cichlids, Hawaiian silverswords, and other icons of adaptive
radiation may be the tip of an evolutionary iceberg; to many prominent biologists, they are
particularly remarkable examples of a phenomenon that may account for the “entire ascent of
life” (Mayr 2001, Raup & Stanley 1971, Simpson 1953, Stebbins 1974, Wright 1982). Indeed,
adaptive radiation may be the primary manifestation of Darwin’s “principle of divergence” (Haas
& Simpson 1946, Kohn 1981, Ridley 2004) and the expected response of an evolving lineage
to natural selection and ecological opportunity. The importance of adaptive radiation, however,
has always been challenged by uncertainty and disagreement regarding some rather fundamental
questions (Futuyma 2003, Givnish 1997, Harder 2001, Olson & Arroyo-Santos 2009, Schluter
2000): What, exactly, is adaptive radiation, and how can it be diagnosed in nature? Is adaptive
radiation a common mode of biological diversification or merely an unusual phenomenon
restricted to a few well-studied clades? What factors determine the occurrence and outcome of
adaptive radiation? To what degree is adaptive radiation a predictable phenomenon?
Today, a new generation of theoretical, experimental, and integrative phylogenetic analyses
place the answers to all of these important questions within reach (Gavrilets & Losos 2009, Kassen
2009, Losos & Mahler 2010). As these analyses provide perspective that was unavailable to early
architects of adaptive radiation like Osborn (1902), Simpson (1953), and Mayr (1963), they are
fundamentally reshaping our understanding of adaptive radiation and its significance. My purpose
here is to review, and in some cases reconsider, the contribution of phylogenetic analyses to
answering outstanding questions about adaptive radiation.
WHAT IS ADAPTIVE RADIATION AND HOW CAN IT
BE DIAGNOSED IN NATURE?
“Adaptive radiation is what happened on Earth over the past four billion years. But this view is so broad that it
converts a useful concept into a truism, as airy and dizzying as vodka. I recommend the narrow view, which is
focused and pungent, like gin.” —David Quammen (1996)
Adaptive radiation results when natural selection drives divergence of an ancestral species into
descendants that are better able to exploit ecological opportunity [Dobzhansky 1948, Gavrilets &
Losos 2009, Kassen 2009, Schluter 2000, Simpson 1953, Wright 1982; see also Losos (2010) for
a recent review of ecological opportunity as it relates to adaptive radiation]. In this sense, adaptive
radiation is analogous to the principle of divergence that Darwin (1859, p. 112) introduced when
he suggested that “the more diversified the descendants from any one species become in structure,
constitution, and habits, by so much will they be better enabled to seize on many and widely
diversified places in the polity of nature, and so be enabled to increase in numbers.” Like the
principle of divergence, adaptive radiation is fundamentally distinct from adaptation via natural
selection; natural selection results in adaptations that improve the fitness of a given population
from one generation to the next, whereas adaptive radiation results in species that possess different
types of adaptations.
Although the growing body of work on adaptive radiation implies a phenomenon that is both
real and important, efforts to define and diagnose it have been marked by controversy [reviewed by
Givnish (1997), Losos (2009), Olson & Arroyo-Santos (2009)]. Is it simply divergence of related
species into a variety of distinct ecological roles (Futuyma 1997, Givnish 1997, Mayr 1963) or is
it restricted to extraordinarily rapid or prolific diversification (Futuyma 2003, Losos & Mahler
2010, Schluter 2000, Simpson 1953, Stanley 1979)? Does adaptive radiation describe a distinct and
broadly important biological phenomenon or merely an interesting pattern of diversity (Losos &
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Mahler 2010, Olson & Arroyo-Santos 2009)? My purposes for revisiting these controversies are
threefold. First, persistent disagreement challenges the status of adaptive radiation as a meaningful
and important concept (Harder 2001, Olson & Arroyo-Santos 2009). Second, I argue that, in spite
of their differences, modern perspectives on adaptive radiation have more in common than they do
in conflict and are often burdened by unnecessary qualifications. Finally, I show how phylogenetic
analyses are providing new perspectives on the meaning and signficance of adaptive radiation, and
reinforcing its standing as the predominant explanation for macroevolutionary diversification.
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The Three Key Features of Adaptive Radiation
All modern definitions of adaptive radiation share two principal features: multiplication of
species and adaptive diversification (Givnish 1997, Losos 2009, Schluter 2000). The first feature
distinguishes adaptive radiation from diversification within a single species and from the assembly
of communities composed of descendants from multiple, evolutionarily distinct lineages. The
second feature represents the adaptation in adaptive radiation. Together, these two features
encompass the widely agreed upon notion that adaptation in the absence of speciation is not adaptive radiation, nor is speciation without adaptation. Indeed, speciation and adaptation are thought
to be intimately linked during adaptive radiation; whether speciation occurs prior to adaptive
divergence or as a direct result of adaptive divergence, it is considered essential to the evolution
and maintenance of ecological and phenotypic diversity (see Futuyma 1989). A third feature
included in some definitions of adaptive radiation—extraordinary diversification—is less easily
characterized and considerably more controversial. Indeed, the nature of extraordinary diversification, and why such diversification should be considered integral to adaptive radiation, has been a
source of persistent controversy (Givnish 1997, Losos & Mahler 2010, Sanderson 1998, Schluter
2000).
To consider the contribution of phylogenetic analyses to defining and diagnosing adaptive radiation, I focus on operational criteria used to test each of the three features discussed
above: (a) multiplication of species and common descent, (b) adaptation via natural selection, and
(c) extraordinary diversification. Together, these criteria constitute a comprehensive test of adaptive radiation similar to that proposed by Schluter (2000).
Criterion 1: Multiplication of species and common descent. Although reconstructing patterns of common descent is a straightforward application of phylogenetic trees, the type of common
descent expected for adaptive radiations can be deceptively complex. On the one hand, the suggestion that life as a whole shares a common ancestor and therefore represents an adaptive radiation
seems overly broad. On the other hand, requiring that clades undergoing adaptive radiation include all descendants of a particular common ancestor is overly restrictive; as noted by Schluter
(2000, p. 11), “[n]o theory of adaptive radiation predicts monophyly.”
To understand why adaptive radiation cannot be diagnosed too broadly, it is important to
remember that it involves divergence of species and associated adaptations in response to natural
selection and ecological opportunity. In practice, this process can only be investigated among relatively closely related species that demonstrate some degree of geographic and ecological cohesion
(that is, access to shared opportunity). Although diversification that occurred deeper in the tree
of life may be the result of adaptive radiation, the degree to which diversification has occurred
subsequently can make it difficult to test this hypothesis directly. At some level, adaptive radiation
must be distinguished from processes like species sorting and community assembly.
The fact that adaptive radiation can only be investigated directly among recently diverged
species does not trivialize its importance or generality, just as our inability to directly observe each
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stage in the evolution of the vertebrate eye does not trivialize natural selection. If it can be shown
that diversification among closely related species tends to result from adaptive radiation, it may
be reasonable to suggest that earlier diversification events involved the same process and perhaps
even to suggest that most of life is the result of adaptive radiation. Instead of viewing adaptive
radiation in “broad” and “narrow” senses (sensu Schluter 2000), however, it may be better to
simply recognize that the hierarchical nature of evolutionary diversification makes it increasingly
difficult to diagnose adaptive radiation as we move deeper into the tree of life.
Even when investigating the process of adaptive radiation among closely related species, one
must be careful about interpreting common descent too narrowly or too broadly. Because adaptive
radiation results from access to shared opportunity, the application of the common descent criterion is intimately linked to the geographic distribution and historical biogeography of a particular
ancestor’s descendants. Although adaptive radiation is most easily diagnosed when a geographically circumscribed lineage diversifies entirely in situ, this pattern lies at one end of a continuum
that includes some degree of dispersal away from, or even into, the region of interest. Two iconic
examples of adaptive radiation serve to illustrate this point.
Seven of the nine anole lizard species found on Puerto Rico, including representatives of three
distinct types of microhabitat specialists, form part of a well-supported clade (Brandley & De
Queiroz 2004). The fact that this clade also includes three species endemic to smaller islands
off the coast of Puerto Rico does not reject the hypothesis of adaptive radiation because these
species represent clear cases of dispersal and subsequent differentiation of colonists from mainland
Puerto Rico (Rodrı́guez-Robles et al. 2007). A similar pattern is observed among African Rift Lake
cichlid fishes, where some lake radiations—such as Lake Tanganyika’s endemic Lamprologini—
are rendered nonmonophyletic by one or more relatively unsuccessful riverine lineages (Day et al.
2007). In both anoles and cichlids, species that disperse away from an ongoing radiation can even
go on to undergo adaptive radiations of their own (Genner et al. 2007, Nicholson et al. 2005). If
it can be shown that some taxa clearly dispersed away from the location of the initial radiation and
were not involved in its subsequent diversification, it is generally reasonable to prune these taxa
and investigate adaptive radiation in the clade that diversified in situ (Figure 1).
This situation becomes more complicated when the members of a putative radiation result
from numerous independent colonization events. This situation also applies to Puerto Rico’s
anole fauna, which includes twig and crown-giant microhabitat specialists that are more closely
related to anoles on other islands than they are to other Puerto Rican species. Although the origin
of Puerto Rico’s twig species remains unclear, the crown-giant appears to be a relatively recent
colonist from crown-giant stock on Hispaniola; thus, this species likely did not evolve the crowngiant condition as a result of processes occurring within Puerto Rico. Lake Tanganyika’s cichlids
share a similarly complex origin and appear to result from numerous independent colonization
events, some of which involved species that arrived preadapted for a particular niche rather than
diverging into this niche as a result of in situ adaptive radiation (Koblmüller et al. 2008).
Although clades resulting exclusively from in situ diversification provide the most simple and direct window on adaptive radiation, consideration of interactions among related subclades evolving
in parallel are required to understand many species-rich radiations; in some cases, more distantly
related species may actually interact more strongly with one another than with more closely related
species (Losos et al. 2003). Detailed phylogenetic studies of biogeography and adaptive evolution
are required to ascertain the relative contributions of in situ diversification via adaptive radiation
versus colonization and species sorting.
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Criterion 2: Adaptation. Adaptation can be diagnosed using two distinct approaches: (a) functional or experimental studies of trait utility, and (b) comparative analyses that identify significant
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Region 1
Region 2
Figure 1
Assessing common descent in adaptive radiation. The shapes of icons at the tips of this tree indicate
ecologically and morphologically distinct forms. The colors of these shapes indicate the geographic region
that each species can be found in. In this case, the fauna in region 1 (red ) may be a product of adaptive
radiation, whereas the fauna in region 2 ( yellow) are not because the fact that they are codistributed in this
region may be due simply to ecological sorting of species that evolved elsewhere.
phenotype-environment correlation (Schluter 2000). Although the first approach does not rely
directly on phylogenetic analyses, the second requires phylogenetic insight. The reason for this
is that nonphylogenetic tests can yield significant correlations that are not sustained when nonindependence of taxa due to common descent is taken into account (Harvey & Pagel 1991).
Felsenstein (1985) provided the first statistical solution to phylogenetic nonindependence when
he introduced phylogenetically independent contrasts (PIC), which uses a Brownian model of trait
evolution to transform nonindependent tip values into a set of independent comparisons across
a phylogeny’s tips and internal nodes. Some of the earliest studies to use PIC were focused on
the identification of phenotype-environment correlations during adaptive radiation (Losos 1990).
More recent examples include Whittall & Hodges (2007) use of PIC to recover a significant
association between the length of floral nectar spurs and three distinct pollinator syndromes
during the adaptive radiation of columbine flowers.
Although PIC remains widely used, methods for testing adaptation in a phylogenetic context
have expanded dramatically over the past quarter century. Some of these methods may be viewed
as extensions of the PIC approach and are also generally restricted to analyses of continuously
coded traits. Phylogenetic generalized least squares (PGLS) (Martins 1997), for example, includes
PIC as a special case but permits identification of phenotype-environment correlation under nonBrownian models of character evolution. The Ornstein-Uhlenbeck (OU) model has attracted the
most attention because it may more accurately reflect evolution of traits evolving under natural
selection by placing some constraint on divergence from optimal trait values (Butler & King 2004).
Clabaut et al. (2007), for example, recently used PGLS and the OU model to identify phenotypic
traits associated with specific feeding preferences in cichlid fish. The model for trait evolution
proposed by Price (1997), in which species undergoing adaptive radiation fill a fixed niche space,
provides another alternative for testing adaptation of continuously coded traits in a phylogenetic
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context (Harvey & Rambaut 2000). Developing in parallel with PIC and related methods are
alternative analytical frameworks that permit similar tests with discretely coded traits (Pagel 1999,
Schluter et al. 1997).
Given the breadth of available methods and the rapidly expanding availability of phylogenetic
trees, access to detailed data on phenotypic and ecological variation is quickly becoming the
rate-limiting step for tests of adaptation during adaptive radiation. Although much of this data
must be gathered with a “boots on the ground” approach, newly available bioinformatic databases
provide one possible shortcut. Geographic information systems (GIS) data layers composed of
environmental and climatological data, for example, may be combined with existing museum
records of species distributions to quickly identify the environmental features typical of a particular
population or species (Graham et al. 2004). Combined with phenotypic data, this environmental
niche data permits widespread assessment of one type of phenotype-environment correlation
during adaptive radiation. Although methods for analyzing this GIS data in a phylogenetic context
remain in their infancy, this is an active area of research (Warren et al. 2008).
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Criterion 3: Extraordinary diversification. Simpson (1953, p. 223) codified the notion that
diversification during adaptive radiation is extraordinary when he suggested that it involves “more
or less simultaneous divergence of multiple lines.” In the years since, students of adaptive radiation
have proposed a variety of alternative explanations for how and why diversification during adaptive radiation might be extraordinary [reviewed by Givnish (1997) and Losos & Mahler (2010)].
I consider how phylogenies can be used to address two distinct (albeit frequently conflated) perspectives before concluding with a discussion of whether extraordinary diversification should be
considered an integral feature of adaptive radiation.
Temporal burst of diversification. Simpson’s (1953) influential model of adaptive radiation suggests that a burst of diversification will be associated with access to new dimensions of ecological
opportunity before slowing as these opportunities are filled. Under this model, extraordinary diversification is diagnosed longitudinally by identifying particularly rapid bursts of diversification
during the course of a single clade’s history. Although once restricted to paleontological analyses of
groups with reasonably comprehensive fossil records (e.g., Sepkoski 1998), phylogenetic analyses
dramatically expand the scope of tests for bursts of diversification by permitting investigation of
extant groups with little or no fossil records (Harmon et al. 2003, 2008; Nee et al. 1992; O’Meara
et al. 2006; Paradis 1997; Pybus & Harvey 2000; Rabosky & Lovette 2008a; Wollenberg et al.
1996; Zink & Slowinski 1995) (Figure 2a).
A range of phylogenetic methods are available to identify temporal bursts of species diversification, all of which involve two basic steps: (a) generation of a well-resolved, comprehensively
sampled, and time-calibrated phylogeny, and (b) comparison of the internode distances in this phylogeny to expectations under simple model(s) of the diversification process (Nee et al. 1992, Pagel
1999, Paradis 1997, Rabosky & Lovette 2008, Wollenberg et al. 1996). Models involving constant
diversification produce similar internode distances throughout the tree, whereas those involving
particularly rapid rates of cladogenesis result in relatively short internode distances in some part
of the tree. Numerous recent studies reject the null hypothesis of rate constancy and recover
evidence for temporal bursts of species diversification (Barraclough & Vogler 2002, Phillimore
& Price 2008, Rabosky & Lovette 2008). As these methods mature, potential problems like the
influence of extinction and inaccurate models of molecular evolution are being actively debated
(Rabosky & Lovette 2009, Revell et al. 2005).
In any case, tests for bursts of species diversification address only half of Simpson’s model,
which also predicts a burst of adaptive differentiation. Phylogenetic tests for temporal bursts of
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a
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−70
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Figure 2
Alternative approaches to the diagnosis of rapid adaptive radiation. In both cases, extraordinary adaptive radiations are indicated by
green bars, whereas clades that did not experience extraordinary diversification are in blue. (a) Extraordinary diversification diagnosed
as a burst at some point in the clade’s history. (b) Extraordinary diversification diagnosed when one clade is significantly more species
rich than the other.
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adaptive phenotypic differentiation are now available, albeit less frequently implemented than
tests for bursts of species diversification. Using a variety of different methods, temporal bursts
are recovered in some, but not all, putative examples of adaptive radiation (Agrawal et al. 2009;
Freckleton & Harvey 2006; Harmon et al. 2003, 2008; Mahler et al. 2010; O’Meara et al. 2006).
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Extraordinarily diverse relative to other clades. A second widely held perspective on extraordinary diversification suggests that adaptive radiation involves exceptional diversity or exceptional
rates of diversification (either taxonomically, phenotypically, or some combination of the two) [reviewed by Givnish (1997), Losos & Mahler (2010)]. Most recently, Losos & Mahler (2010) suggest
“the term adaptive radiation should be reserved for those clades exhibiting an exceptional degree
of ecological and phenotypic disparity.” This type of extraordinary diversity is often conflated
with temporal bursts of diversification and might result when some clades experience a temporal
burst of diversification while others do not; its diagnosis, however, requires comparisons among
clades rather than longitudinal studies within a given clade (Figure 2b).
Phylogenetic information is essential to identifying clades that experience exceptional diversification. To avoid age-related biases, early analyses focused on comparing clades that were known
to be similar in age. Tests for extraordinarily high levels of species diversity, for example, were
initially applied to sister groups (which are the same age by definition) (Slowinski & Guyer 1989).
A similar approach has been used to identify extraordinarily morphologically diverse clades; Losos
& Miles (2002), for example, identify exceptional levels of morphological disparity among clades
of iguanian lizards that were judged to be the same age because they diverged from a polytomy.
More recently, comparisons of absolute rates of diversification are used to relax the requirement
that the clades being compared be the same age (Maddison et al. 2007, Magallón & Sanderson
2001, Moore & Donoghue 2009, Ree 2005). Ree (2005), for example, used a Bayesian phylogenetic approach to identify a significantly elevated rate of species diversification in the plant genus
Aquilegia. Meanwhile, Collar et al. (2005) asked whether morphological disparity accumulates at
different rates in clades of centrarchid fish using a well-sampled phylogenetic tree and a Brownian
model of character evolution. As studies of evolutionary rates mature, it is essential to consider
biases that might be introduced when the simple null model of constant diversification over time
is rejected, as is likely to be the case when bursts of diversification occur in association with access
to new opportunity (Rabosky 2009).
Are adaptive radiations extraordinary? In spite of their increasing effectiveness and popularity,
phylogenetic tests for extraordinary diversification are incapable of resolving debate over whether
such diversification is required, merely expected, or entirely unrelated to adaptive radiation. For
this reason, we must consider the underlying justification for considering some form of extraordinary diversification an integral feature of adaptive radiation.
Although the temporal burst model of adaptive radiation remains one of Simpson’s (1953)
most enduring legacies, the original justification for this model relies on another of his views that
was never widely accepted or tested; namely, his assertion that ecological opportunity tends to be
discontinuously distributed and defined by distinct “adaptive zones.” Simpson thought adaptive
radiation would be accompanied by a temporal burst of diversification due to the intrinsically
discontinuous nature of the underlying opportunity, not because it involved any processes distinct
from those contributing to more gradual diversification. As noted by Gould (2002), the accelerated
frequency of branching events during adaptive radiation does “not affect the modality of change.”
The view that adaptive radiations must experience exceptional diversification relative to other
groups also lacks an established mechanistic explanation. In some cases, this view contends only
that adaptive radiations are a special pattern of diversity, whose meaning depends on our ability to
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distinguish them from ordinary diversification (Losos & Mahler 2010). In other cases, exceptional
diversification is expected because underlying speciation or adaptation tends to occur particularly
quickly during adaptive radiation (Schluter 2000, Kassen 2009). Schluter’s (2000) ecological theory
of adaptive radiation, for example, suggests that the time for speciation, rather than the interval
between speciation or extinction events, is rapid during adaptive radiation due to the prevalence of
ecological speciation (that is, speciation resulting from divergent natural selection). Although this
model requires further empirical consideration, its generality relies on several controversial and
largely untested assumptions (e.g., that speciation during adaptive radiation is primarily ecological,
that ecological speciation is correlated with particularly rapid times for speciation, and that the
time for speciation is the rate-limiting step in adaptive radiation).
Regardless of which perspective is favored, considering extraordinary diversification integral
to adaptive radiation may challenge the term’s status as a well-defined biological phenomenon and
require that it be diagnosed by arbitrarily dividing biological continua (Olson & Arroyo-Santos
2009). Before concluding that adaptive radiation is merely a metaphor for explosive diversification
that has outlived its usefulness (Olson & Arroyo-Santos 2009), however, we should revisit questions
about whether it is necessary to include extraordinary diversification in definitions of adaptive
radiation (see also Givnish 1997, Losos & Mahler 2010, Sanderson 1998).
Some researchers suggest that removing extraordinary diversification would result in a term
that can be applied so broadly that it becomes meaningless and perhaps even tautological (Losos
& Mahler 2010). This argument, however, is fallacious if adaptive radiation is viewed as a process.
Indeed, processes with a broad explanatory scope are often more meaningful and interesting than
those with a more limited scope; one would never argue, for example, that natural selection is so
prevalent that it becomes meaningless. Moreover, adaptive radiation without extraordinary diversification and defined by divergence of species and associated adaptations resulting from natural
selection and ecological opportunity is not so broadly conceived as to be tautological because
biologically plausible alternatives can, and do, exist (e.g., nonadaptive radiation and phenotypic
plasticity) (Kozak et al. 2006, Rundell & Price 2009, Sanderson 1998).
If adaptive radiation is viewed as a process, extraordinary diversification also does not appear
necessary to distinguish it from related evolutionary phenomena. Adaptive radiation is distinguished from the more general process of diversification (whether it be morphological, ecological,
or taxonomic) by the importance it assigns to the linkage between taxonomic and adaptive divergence. Adaptive radiation is also distinct from ecological speciation; indeed, some models suggest
that speciation during adaptive radiation is largely nonecological (Grant & Grant 2008, Losos &
Mahler 2010, Rundell & Price 2009).
In addition to setting the stage for re-establishment of adaptive radiation as a distinct biological
phenomenon of sweeping importance, excluding extraordinary diversification from its definition
may resolve persistent conflict over which clades should be recognized as the outcome of adaptive
radiation. Although some researchers, for example, view columbines as a classic example of adaptive
radiation, Losos (2009) suggests that they simply are not diverse enough to qualify. Other iconic
examples of adaptive radiation, like the two species radiations of sticklebacks and other fish in
postglacial lakes, have also been denied status as full-blown adaptive radiations by definitions that
require extraordinary diversification (Losos 2010).
Perhaps most importantly, leaving extraordinary diversification out of the definition of adaptive
radiation opens the door to a more general, and less controversial, theory. Although some forms
of extraordinary diversification may yet prove to be general features of adaptive radiation, it seems
unwise to limit the scope of adaptive radiation with an unnecessary qualifier just as general theories
accounting for divergence of species and associated adaptations, as well as the expected course of
such divergence events, are emerging (see also Givnish 1997). Taking a broad view of adaptive
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radiation, I consider below how phylogenetic studies can be used to identify patterns of diversity
resulting from adaptive radiation that provide insight on the nature of the underlying process.
WHAT FACTORS DETERMINE THE OCCURRENCE AND SCOPE
OF ADAPTIVE RADIATION?
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The fact that ecological opportunity is a complex and intrinsically dynamic entity challenges efforts
to predict the nature of adaptive radiation (Grant 2001, Losos 2010). Nevertheless, integrative
phylogenetic analyses can diagnose patterns of diversification that provide clues about the catalysts
and expected outcomes of adaptive radiation. Temporal bursts of diversification, for example,
suggest that diversification is limited by available opportunity or a given group’s ability to exploit
this opportunity (Rabosky 2009). In reviewing phylogenetic insights into the response of adaptive
radiation to ecological opportunity, I follow Simpson (1953) by recognizing the need for access
to three distinct types of ecological opportunity: physical, ecological, and evolutionary.
Access to physical opportunities means simply that radiations must occur where opportunity
exists. Ecological access, meanwhile, requires that opportunities are not already being exploited
by competitively superior species. An abundance of evidence supports the importance of access
to ecological and physical opportunities for adaptive radiation, with the best-known examples involving radiation following colonization of isolated islands or lakes (Grant & Grant 2008, Kocher
2004, Losos 2009). With the aid of phylogenetic analyses, it is also possible to assess how the extent
of adaptive radiation is likely to vary in response to variation in physical and ecological opportunity. Recent studies, for example, provide an evolutionary perspective on the well-established
relationship between area and species diversity [reviewed by Losos & Parent (2009)]. Among
adaptive radiations of Greater Antillean anoles, the species-area relationship appears to result
from a correlation between speciation rate and island area. The situation in bulimulid snails in the
Galapagos is somewhat more complicated and provides evidence for the contribution of both geographic and ecological factors; in these snails, species diversification appears to be dictated partly
by each island’s plant diversity, with greater plant diversity thought to provide “more opportunity
for speciation and species differentiation.”
In addition to geographic and ecological access, the occurrence and extent of adaptive radiation
depend on the availability of evolutionary adaptations or preadaptations. Most iconic examples
of adaptive radiation are thought to possess one or more so-called key innovations, which promote diversification by providing access to new dimensions of opportunity or by enhancing the
likelihood of speciation events within a given clade (Galis 2001). Potential examples include the
pharyngeal jaw in cichlids (Kocher 2004), toe pads in Anolis (Losos 2009), and nectar spurs in
columbines (Ree 2005). Key innovations and their impacts on adaptive radiation, however, have
always been controversial because they are difficult to diagnose and generalize and often lack
mechanistic explanations (Cracraft 1990, Galis 2001). Consider the example of pharyngeal jaws in
fish; although the pharyngeal jaw has long been considered a key innovation in African Rift Lake
cichlids, the reasons for thinking that this trait will cause enhanced diversification are not entirely
clear (Galis 2001). Moreover, evolution of the pharyngeal jaw may not always be a catalyst for
diversification; in labrid fish, for example, diversification may be more closely tied to the evolution
of extreme sexual dichromatism than it is to the evolution of the pharyngeal jaw (Alfaro et al.
2009). It may often be the case that numerous innovations are associated with diversification of
the most species-rich adaptive radiations.
Because all three types of access—physical, ecological, and evolutionary—are required for
radiation, we should not be surprised that efforts to identify the cause for adaptive radiation often
yield inconclusive or inconsistent conclusions. The ability to quantify ecological opportunity
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independently of the organisms that exploit it would certainly be a welcome development (Losos
& Mahler 2010), but this notoriously difficult challenge should not distract attention from the
lessons that can be learned from realized adaptive radiations.
TO WHAT DEGREE IS ECOLOGICAL DIVERSIFICATION DURING
ADAPTIVE RADIATION PREDICTABLE?
The cases of parallel radiation (e.g., Greater Antillean anoles, fishes in postglacial lakes) are as exquisitely
appealing as great works of art, but whether or not they are equally exceptional remains to be seen.
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—Futuyma 2003
Adaptive radiations have long provided one of the main challenges to Gould’s (1989) famous
assertion that replaying of the tape of life is unlikely to yield a similar outcome. Indeed, replicate
radiations that independently evolve ecologically similar forms were a central feature of Osborn’s
(1902) original law of adaptive radiation. Osborn (1934) identified numerous remarkable examples
of replicate radiation in the fossil record, and even thought that they required a non-Darwinian
explanation; his ill-fated theory of aristogenesis postulated that aristogenes deterministically drive
organisms toward biomechanical optima. Today, of course, replicate radiations are viewed as
powerful evidence that Darwinian natural selection acting on organisms exposed to similar adaptive
landscapes can sometimes overwhelm historical and ecological contingencies (Losos 2009).
Some of the most impressive examples of replicate radiation have been revealed with the aid
of phylogenetic methods, including fish in postglacial lakes (Snorrason & Skulason 2004), Anolis
lizards on Greater Antillean islands (Losos 2009), and cichlid fish in African Rift Lakes (Kocher
2004). In each of these cases, similar ecological specialists evolve repeatedly on isolated islands
or lakes, resulting in some degree of species-for-species matching among evolutionarily independent radiations (see Schluter 1990). Sticklebacks, charr, whitefish, and trout that colonize isolated
postglacial lakes across the Northern Hemisphere, for example, repeatedly diverge into benthic
and limnetic specialists (Snorrason & Skulason 2004). Among Greater Antillean Anolis lizards and
African Rift Lake cichlids, replicate radiation is even more striking, with evolutionarily isolated radiations including five or more replicated specialists [reviewed by Kocher (2004) and Losos (2009)].
Although replicate radiations as impressive as those seen in Anolis lizards and African Rift Lake
cichlids may be exceptional, recent phylogenetic studies have uncovered numerous additional examples with some degree of species-for-species matching. Snails (Mandarina) from Japan’s Bonin
Islands have repeatedly evolved similar arboreal, semiarboreal, sheltered ground, and exposed
ground habitat specialists (Chiba 2004). Web-less, spiny-legged, long-jawed spider radiations
on Hawaiian islands (Tetragnatha) include replicated ecomorphs, and related orb-weaving spiders on the same islands include replicated web architectures (Blackledge & Gillespie 2004,
Gillespie 2004). Ecologically and geographically distinct radiations of lilies (Calochortus) across
western North America have repeatedly evolved strikingly similar floral morphologies (Patterson
& Givnish 2004). The freshwater isopod species Asellus aquaticus appears to be on a similar course
as fish in postglacial lakes, having rapidly and repeatedly evolved into distinct reed and stonewort
ecotypes following invasion of Swedish lakes (Eroukhmanoff et al. 2009). At a deeper level, radiations of placental mammals from Laurasia and Africa include superficially similar aquatic, ungulate,
and insectivore-like forms (Madsen et al. 2001). Similarly, communities of iguanid and agamid
desert lizards in western North America and Australia, respectively, include ecologically similar
arboreal, semiarboreal, saxicolous, ground-dwelling species, which sometimes correspond with
similar underlying morphological adaptations (Melville et al. 2006).
Additional examples of replicate radiations with species-for-species matching likely remain to
be uncovered. In some cases, examples of replication likely remain masked by traditional taxonomic
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arrangements that group organisms by phenotypic traits associated with ecological specialization.
Relatively recent molecular phylogenetic analyses of the well-known bat genus Myotis, for example,
reveal that three major subgenera diagnosed on the basis of overall phenotypic similarity actually
correspond with distinct modes of food procurement and associated morphological adaptations
that have evolved independently in Palaearctic, New World, Asian, and African radiations (Ruedi
& Mayer 2001). Similarly, ranid frog genera defined on the basis of phenotypic similarities have
been shown to be nonmonophyletic aggregations of species with similar ecological syndromes
that evolved independently in Asia and Madagascar (Bossuyt & Milinkovitch 2000). Many more
such examples likely remain to be uncovered, particularly among groups like plants and insects
whose vast diversity remains relatively untouched by detailed species-level phylogenetic analyses.
Regardless of how common replicate radiations with species-for-species matching may be, their
phylogenetic scope is always somewhat limited (Losos 2009). We may be able to predict how an
African haplochromine cichlid is likely to respond to a vacant crater lake, or how an anole will diversify on a large Caribbean island, but can we also identify broader generalities to the patterns of ecological specialization that evolve during adaptive radiation? A number of recent phylogenetic and
theoretical studies suggest that this may indeed be the case [reviewed by Gavrilets & Losos (2009)].
One long-standing general model for ecological diversification during adaptive radiation predicts the evolution of specialists from a generalist ancestor [reviewed by Schluter (2000)]. Recent
phylogenetic comparative analyses have tested this prediction by asking (a) whether the ancestors
of radiations tend to be generalists or specialists and (b) whether transitions from the generalists to
specialists are more likely than the converse (Nosil & Mooers 2005, Schluter 2000). The results
of these studies are largely equivocal, suggesting that “a trend toward specialization is sometimes
seen but is not universal or widespread” (Schluter 2000, p. 43). It may be important, however, to
re-evaluate previous work on this subject using models of character evolution that consider the
impact of the generalist and specialist categories on rates of speciation and extinction (Goldberg
& Igic 2008, Maddison et al. 2007).
Regardless of prevalence, the generalist to a specialist model is also likely to be of limited
significance; as noted by Schluter (2000, p. 49), “continuous spread to new environments, and not
specialization, is the dominant trend of adaptive radiation.” A number of recently developed models
suggest that diversification during adaptive radiation may occur along predictable ecological axes
and in a predictable sequence (Ackerly et al. 2006, Schluter 2000, Streelman & Danley 2003). The
habitat first rule (HFR), for example, suggests that birds tend to diversify first into habitat specialists
(e.g., mountain versus lowland) and later into dietary specialists within a given habitat [reviewed
by Schluter (2000)]. The general vertebrate model (GVM), meanwhile, suggests a similar scenario
for diverse radiations of fish, lizards, and birds, adding divergence of sexually selected traits as a
possible third axis of specialization subsequent to habitat and dietary divergence (Streelman &
Danley 2003).
The superficial similarity of these scenarios, however, belies deep conflict in their underlying
data and highlights an important limitation of phylogenetic inference (Figure 3). In studies used
to support the HFR, distantly related species differed along a dietary axis, whereas closely related
species tended to differ in habitat. Groups used to support the GVM, meanwhile, exhibit the
opposite pattern, with distantly related clades differing along a habitat axis, whereas closely related
species tended to differ in diet. That opposing patterns of diversification have led to similar
diversification scenarios can be attributed to assumptions made about the nature of rapidly evolving
traits (which tend to differ among closely related species). In the HFR, habitat first diversification
is inferred after assuming that traits differing among closely related species are also likely to
have diverged during earlier phases of the radiation. This assumption of rate constancy is widely
employed by maximum likelihood and Bayesian methods for character reconstruction. Habitat
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a Habitat first rule
b General vertebrate model
Habitat
Diet
Habitat
Diet
Figure 3
Alternative approaches to reconstructing the history of ecological specialization during adaptive radiation.
Different shapes indicate the two ecological axes under consideration, with circles indicating habitat and
squares indicating diet. Different colors within each shape indicate alternative specialist forms along each
ecological axis. The known ancestral condition is indicated at the base of the tree. (a) In examples used to
support the habitat first rule, habitat divergence is observed between closely related species pairs that share
similar diets. This model infers habitat divergence along the basal split (prior to dietary divergence
associated with the same split) after assuming that the same type of differences observed among closely
related species likely occurred in association with earlier speciation events. (b) In examples used to support
the general vertebrate model, closely related species share similar habitats while differing in dietary
preference. This model infers habitat divergence along the basal split after assuming the best solution is the
one that minimizes the number of reconstructed changes.
first diversification is inferred by the GVM, meanwhile, after assuming that the best reconstruction
is the one that minimizes the total number of character changes. This assumption corresponds
with classic parsimony-based methods for character reconstruction. Because both rate constancy
and parsimony may be reasonable assumptions when traits exhibit little or no phylogenetic signal,
it is important to carefully consider the influence of these alternative assumptions on historical
inference. In some cases, other lines of evidence, like the factors underlying speciation events
during adaptive radiation, may provide additional clues about the likely sequence of diversification
(Price 2007).
Ackerly et al. (2006) developed a new statistical test—the divergence order test, or DOT—that
explicitly incorporates uncertainty of historical inference resulting from the absence of phylogenetic signal. They applied this test to a radiation of live oaks from the western United States
(Caenothus) that appears to have diversified along two distinct habitat axes. One of these axes permits species to occur in local sympatry (α-niche divergence), whereas the other results in species
that occur in regionally distinct macrohabitats (β-niche axis). Ackerly et al.’s (2006) analyses recovered a clear signal of early diversification along the α-niche axis and evidence that β-niche
differentiation tends to occur among closely related species. After recognizing that any efforts to reconstruct the history of β-niche diversification produces an ambiguous conclusion, they appealed
to the constant rate assumption when they suggested that “it is parsimonious to assume that deeper
events also involved [the type of changes observed most recently].” The α-early, β-throughout
model that emerged from these analyses clarified ambiguity in the use of the term habitat and
defined two broadly important niche axes that generalize the axes discussed in previously proposed models. More empirical tests of the α-early, β-throughout model are needed. Although
theoretical work on patterns of ecological diversification remains in its infancy, the available work
supports scenarios similar to the α-early, β-throughout model (Gavrilets & Losos 2009).
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Conclusions on Predictability
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Recent phylogenetic studies suggest that predictable patterns of ecological diversification exist
across a range of phylogenetic scales, from species-for-species matching among closely related radiations to similar patterns of ecological diversification across deeply divergent groups. Although
these results are in line with a growing emphasis on the influence of deterministic events on evolutionary diversification (Conway-Morris 2003, Stern & Orgogozo 2008), further work is needed
to quantify the generality and phylogenetic scope of putatively replicated patterns. Regardless
of how common predictable patterns of ecological diversification may be, they open the door to
integrative insights into the nature of ecological opportunity and the ecological and genetic limits
on adaptive diversification (Kassen 2009, Losos 2010).
CAN THE PHYLOGENETIC HISTORY OF ADAPTIVE
RADIATION BE RECONSTRUCTED?
The last question I address is a fundamental challenge to integrative phylogenetic analyses of
adaptive radiation, which generally depend on detailed species-level phylogenetic trees. Today,
such trees are available for most iconic adaptive radiations as well as a range of lesser-known
examples. Adaptive radiations occurring in Lake Tanganyika, one of Africa’s large Rift Lakes, are
emblematic of this progress, with phylogenies now available not only for this lake’s famous cichlid
fauna [reviewed by Koblmüller et al. (2008)] but also for its lesser-known gastropods (Strong &
Glaubrecht 2008), catfish (Day et al. 2009), crabs (Marijnissen et al. 2008), and prawns (Fryer 2006).
Nevertheless, phylogenetic trees for some radiations remain poorly resolved, often in spite of
considerable effort. Polytomies and poorly supported nodes, for example, have long plagued phylogenetic analyses of such well-known radiations as Galapagos finches (Petren et al. 1999), Hawaiian
silverswords (Baldwin & Sanderson 1998), Dendroica warblers (Rabosky & Lovette 2008), Anolis
lizards ( Jackman et al. 1999), and African cichlids (Kocher 2004). These problems are most frequently attributed to the temporal bursts of species diversification associated with some examples
of adaptive radiation ( Jackman et al. 1999, Poe & Chubb 2004). The closely spaced branching
events that tend to result from such bursts (that is, soft polytomies) are notoriously difficult to
resolve due to three specific problems: (a) insufficient time for accumulation of diagnostic substitutions, (b) long-branch attraction, and (c) incomplete lineage sorting (Rokas & Carroll 2006,
Wiens et al. 2008).
Accumulation of additional phylogenetically informative data is a straightforward solution to
the first problem. Today, long-standing limits on the acquisition of additional data are rapidly
eroding as genomic data permits development of large suites of phylogenetically informative markers (Backström et al. 2008, Thomson et al. 2008, Townsend et al. 2008). Thomson et al. (2008),
for example, used the genomic DNA sampled from bacterial artificial chromosome (BAC) end sequences from the painted turtle to develop primers capable of amplifying novel loci across turtles.
Backström et al. (2008), meanwhile, developed PCR primers for hundreds of loci spread across
the avian genome after identifying orthologous protein-coding regions in genomic sequences for
the chicken and the zebra finch. Whole genome sequencing efforts promise to provide many more
new loci, as well as critical information about the genomic locations of these loci; such projects
are complete or underway for representatives of several iconic adaptive radiations, including the
threespine stickleback (Gasterosteus aculeatus), an anole (Anolis carolinensis), a columbine (Aquilegia
formosa), and several species of African cichlids.
Recent studies suggest that additional data can improve resolution of some polytomies attributed to rapid species diversification. Just a few years after Rokas et al. (2005) predicted that the
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short branches among basal metazoans would be irretrievable regardless of the amount of data employed, Dunn et al. (2008) resolved these relationships with high levels of support using a 39.9-Mb
data set composed of expressed sequence tags (ESTs) from 29 taxa representing 21 phyla. Similarly, Hackett et al. (2008) were able to resolve long-controversial basal bird relationships using a
32,000-bp data set comprising 19 genes from 169 species. Analysis of a 20-locus, 50-species data
set was also able to recover some previously controversial or poorly supported relationships among
snakes, although other nodes in the snake phylogeny remain problematic (Wiens et al. 2008).
The value of adding more data is ultimately limited by the fact that this approach alone is
unable to address the other two phylogenetic problems that result from rapid radiation: long
branch attraction and incomplete lineage sorting. Indeed, increasingly large data sets may actually
become positively misleading when levels of homoplasy are high, as is likely with long-branch
attraction or incomplete lineage sorting (Degnan & Rosenberg 2006, Felsenstein 1978). I focus
on incomplete lineage sorting here because it seems likely to be more broadly problematic (Wiens
et al. 2008).
Incomplete lineage sorting occurs when haplotypes do not coalesce in diverging lineages before
these lineages split again, and results in gene trees that reflect stochastic sorting of ancestral
polymorphisms rather than evolutionary relatedness. Evidence for incomplete lineage sorting
during putative adaptive radiations comes in the form of incongruent gene trees recovered for
groups like Tanganyikan cichlids (Tropheus) (Egger et al. 2007), Hawaiian Laupala crickets (Shaw
2002), and Thomomys gophers (Belfiore et al. 2008). In these cases, standard methods involving
concatenation of multilocus data may recover incorrect relationships with high levels of support
(Belfiore et al. 2008, Degnan & Rosenberg 2006). Efforts to resolve this problem—most recently
involving direct estimation of a species tree from a suite of (possibly conflicting) gene trees—
represent one of the most important recent advances in phylogenetic inference (Ané et al. 2007,
Edwards et al. 2007, Liu & Pearl 2007, Maddison & Knowles 2006). Although application of
these methods remains limited to relatively small data sets due to computational limitations, the
efficiency of these methods continues to improve.
Of course, large multilocus data sets and the new methodologies being developed to analyze
them present analytical challenges of their own. One problem is the amount of missing data typical
of many phylogenomic data sets. The consequences of missing data for standard phylogenetic
analyses remain poorly understood; some analyses suggest that they will not be overly problematic
(Wiens & Moen 2008), whereas others suggest that serious problems are likely (Lemmon et al.
2009). The impact of missing data on newly available species trees from gene trees approaches is
even less well understood.
Another challenge associated with increasingly large data sets—the limits of available computing power—is certainly not a new challenge for phylogeneticists. Today, widely used methods for
Bayesian phylogenetic inference may not be computationally feasible with the largest data sets
(Hackett et al. 2008). Newly developed fast maximum likelihood methods represent one possible solution, but the properties of these methods remain poorly understood relative to Bayesian
analyses (Stamatakis 2006, Zwickl 2006). Whatever methods are used, they are likely to increasingly benefit from the use of centralized parallel computing resources and programs developed to
exploit them to their full potential.
CONCLUSIONS
Modern phylogenetic analyses are enriching and expanding an understanding of adaptive radiation
gained principally from studies of a few iconic examples. Integration of these analyses with paleontological, theoretical, and experimental work is already providing insight into adaptive radiation’s
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core processes and the resulting patterns of diversity. As general theories of adaptive radiation
emerge from this work, it is best to define adaptive radiation broadly as a process analogous to
Darwin’s principle of divergence involving coupled diversification of species and associated adaptations in response to natural selection and ecological opportunity. Although more comprehensive
quantitative tests for adaptive radiation and its outcomes are required, the existing evidence supports the long-held notion that adaptive radiation may be the predominant mode of biological
diversification (Simpson 1953, Raup & Stanley 1971, Stebbins 1974, Wright 1982, Wilson 1999,
Mayr 2001).
DISCLOSURE STATEMENT
Annu. Rev. Ecol. Evol. Syst. 2010.41:251-270. Downloaded from www.annualreviews.org
by Dr. Diego Rodriguez on 02/24/12. For personal use only.
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
I thank Brad Shaffer, Luke Harmon, Luke Mahler, Jonathan Losos, Daniel Scantlebury, Anthony
Geneva, Seth Rudman, and Julienne Ng for their thoughtful comments on a previous draft of this
manuscript.
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Contents
Annual Review of
Ecology, Evolution,
and Systematics
Volume 41, 2010
What Animal Breeding Has Taught Us about Evolution
William G. Hill and Mark Kirkpatrick p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
From Graphs to Spatial Graphs
M.R.T. Dale and M.-J. Fortin p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p21
Putting Eggs in One Basket: Ecological and Evolutionary Hypotheses
for Variation in Oviposition-Site Choice
Jeanine M. Refsnider and Fredric J. Janzen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p39
Ecosystem Consequences of Biological Invasions
Joan G. Ehrenfeld p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p59
The Genetic Basis of Sexually Selected Variation
Stephen F. Chenoweth and Katrina McGuigan p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p81
Biotic Homogenization of Inland Seas of the Ponto-Caspian
Tamara Shiganova p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 103
The Effect of Ocean Acidification on Calcifying Organisms in Marine
Ecosystems: An Organism-To-Ecosystem Perspective
Gretchen Hofmann, James P. Barry, Peter J. Edmunds, Ruth D. Gates,
David A. Hutchins, Terrie Klinger, and Mary A. Sewell p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 127
Citizen Science as an Ecological Research Tool: Challenges
and Benefits
Janis L. Dickinson, Benjamin Zuckerberg, and David N. Bonter p p p p p p p p p p p p p p p p p p p p p p p 149
Constant Final Yield
Jacob Weiner and Robert P. Freckleton p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 173
The Ecological and Evolutionary Consequences of Clonality
for Plant Mating
Mario Vallejo-Marı́n, Marcel E. Dorken, and Spencer C.H. Barrett p p p p p p p p p p p p p p p p p p p 193
Divergence with Gene Flow: Models and Data
Catarina Pinho and Jody Hey p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 215
Changing Geographic Distributions of Human Pathogens
Katherine F. Smith and Jean-François Guégan p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 231
v
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Phylogenetic Insights on Adaptive Radiation
Richard E. Glor p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 251
Nectar Robbing: Ecological and Evolutionary Perspectives
Rebecca E. Irwin, Judith L. Bronstein, Jessamyn S. Manson, and Leif Richardson p p p p p 271
Germination, Postgermination Adaptation, and Species
Ecological Ranges
Kathleen Donohue, Rafael Rubio de Casas, Liana Burghardt, Katherine Kovach,
and Charles G. Willis p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 293
Annu. Rev. Ecol. Evol. Syst. 2010.41:251-270. Downloaded from www.annualreviews.org
by Dr. Diego Rodriguez on 02/24/12. For personal use only.
Biodiversity and Climate Change: Integrating Evolutionary
and Ecological Responses of Species and Communities
Sébastien Lavergne, Nicolas Mouquet, Wilfried Thuiller, and Ophélie Ronce p p p p p p p p p p p 321
The Ecological Impact of Biofuels
Joseph E. Fargione, Richard J. Plevin, and Jason D. Hill p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 351
Approximate Bayesian Computation in Evolution and Ecology
Mark A. Beaumont p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 379
Indexes
Cumulative Index of Contributing Authors, Volumes 37–41 p p p p p p p p p p p p p p p p p p p p p p p p p p p 407
Cumulative Index of Chapter Titles, Volumes 37–41 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 410
Errata
An online log of corrections to Annual Review of Ecology, Evolution, and Systematics
articles may be found at http://ecolsys.annualreviews.org/errata.shtml
vi
Contents