3 The Fruit of the Tree of Life Insights into Evolution and Ecology

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Douglas J. Futuyma

A milestone in the history of biology—and indeed of science

and of society—was passed in February 2001, when two

research groups announced completion of a “draft” of the

human genome (International Human Genome Sequencing

Consortium 2001, Venter et al. 2001). Even if some biologists

felt that this event had rather less scientific significance

than the public acclaim might suggest (because, after all,

complete genome sequences had already been published for

quite a few other species), the social and medical implications

are undeniably immense. And for an evolutionary biologist,

the most gratifying aspect of this historic event is that

the leading publications are pervaded with evolutionary interpretation:

“Most human repeat sequence is derived from

transposable elements.” “The monophyletic LINE1 and Alu

lineages are at least 150 and 80 Myr old, respectively.” “[M]ost

protein domains trace at least as far back as a common animal

ancestor.” “[C]onservation of gene order [between human and

mouse] has been used to identify likely orthologues between

the species, particularly when investigating disease phenotypes.”

[All quotations are taken from International Human

Genome Sequencing Consortium (2001).]

An evolutionary perspective has been indispensable for

making any sense of the features of the human genome, simply

because all the characteristics—genomic and phenotypic

alike—of all organisms are the products of evolutionary history.

We thus need to understand, as fully as possible, both

what that history has been (how old are protein domains?)

and what processes have produced it (how did repeat sequences

arise?). These, indeed, have been the two overarching

tasks of the science of evolutionary biology. It should be

obvious that studies of history and of processes should each

support and illuminate the other. Indeed, they do, and much

of the excitement and progress in contemporary evolutionary

biology stems exactly from the interpenetration of process-

oriented and history-oriented research, a subject of this

essay.

The Emergence of a Synthesis

The study of evolutionary history has historically been mostly

the task of the “macroevolutionary” fields of paleontology and

phylogenetic systematics, whereas evolutionary processes

were traditionally viewed through the “microevolutionary”

lenses of population and ecological genetics. As recently as

1988, one could bewail the great schism that has divided the

two great realms of evolutionary biology for much of its

history and urge a meaningful synthesis between them

(Futuyma 1988). Historians of science will some day analyze

how the synthesis of macroevolutionary and microevolutionary

approaches, in which phylogenetic studies play so

critical a role and which is still underway, came about. I

would like to offer a few historical impressions before

sketching some of the ways in which phylogenetics is making

indispensable contributions to the broader fields of evolutionary

biology and ecology.

25

26 The Importance of Knowing the Tree of Life

Before the Modern Synthesis of evolutionary theory, inferring

relationships and erecting classifications in an evolutionary

spirit were viewed as major goals for biology and

motivated paleontology, morphology, and embryology. Many

classifications were developed that were intended to reflect

common ancestry (and, in many cases, appear to have

achieved that goal remarkably successfully). This work was

accompanied by conclusions about the history of character

transformations (e.g., the origin of mammalian auditory ossicles).

During this period, an “eclipse of Darwinism” in which

natural selection suffered ill repute (Bowler 1983), systematic

and paleontological research was neither deeply informed

by, nor contributed much to, understanding of the causal

factors of evolution.

By the 1930s, evolutionary morphology became relegated

to the sidelines by the rise of experimental disciplines such

as genetics (Bowler 1996), and embryology became an experimental

rather than a historically motivated descriptive

discipline. Evolutionary biology was transformed by the

Modern Synthesis, which arrived at a consensus that genetics

supported Darwinism, that natural selection was the most

important cause of evolution, and that “macroevolutionary”

changes are the consequence of cumulative “microevolutionary”

changes. The synthesis could not have occurred without

the contributions of systematists such as Mayr, Rensch,

and Simpson and of the genetically oriented naturalists

Dobzhansky and Stebbins, with their systematic background.

Although the systematists drew on earlier phylogenetic

studies to support their thesis that macroevolution was explainable

by the “neo-Darwinian” synthetic theory [e.g., by

pointing out major changes in form associated with changes

in function (Mayr 1960)], their contributions to the synthesis

arose mostly from their analyses of speciation and intraspecific

variation, rather than phylogeny.

The synthesis unquestionably emphasized evolutionary

processes rather than evolutionary history as the locus of

progress and invigorating challenge, and in this way doubtless

joined the growing trend toward experimental biology in

marginalizing phylogenetic and historical studies. It is undeniable,

however, that few systematists countered by portraying

phylogeny as a rigorous discipline (it wasn’t; that is why

new methods were developed in the 1960s and thereafter) or

by demonstrating that it could contribute to conceptual understanding.

For example, one of the people who inspired me

to study evolution was William L. Brown, Jr., the world’s authority

on ant systematics. Although he was inspiring in his

search to understand evolutionary processes (e.g., Brown and

Wilson 1956, Brown 1959), not once, in my memory, did he

use ants to illustrate, develop, or test hypotheses about evolutionary

processes or history. Many systematists displayed far

less interest in evolutionary processes than he, and phylogenetic

hypotheses were a less conspicuous part of their work

than were description of species and revision of genera. Important

though such contributions are, they seldom conveyed

intellectual excitement or conceptual progress.

The orthodoxies and preoccupations of a field are often

most visible (even if time-lagged) in textbooks, and the few

textbooks of evolution published in the 1960s and 1970s

illustrate how small a role phylogeny played in evolutionary

biology at that time. Both short, elementary paperbacks,

whether authored by nonsystematists (Stebbins 1966, Volpe

1970) or systematists (Savage 1963), and longer undergraduate

textbooks (Dodson 1960, Eaton 1970) figured at most

five phylogenies of real organisms, usually incorporating a

fossil record. The Equidae, based on Simpson, and the “reptiles,”

based on Romer or Colbert, were the usual subjects.

Virtually the only conceptual point illustrated was adaptive

radiation; certainly no suggestions that phylogeny could inform

our understanding of process were made. Perhaps reflecting

the senior author’s later attitude toward systematics,

the major textbook of the 1960s, Ehrlich and Holm’s The

Process of Evolution (1963), contained not a single phylogeny.

Although 8 of the 38 short chapters in Grant’s Organismic

Evolution (1977) treat macroevolution, the only two

phylogenies depicted accompany a description of the adaptive

radiation of Hawaiian honeycreepers and a discussion

of the canonical Hyracotherium-to-Equus “trend.”

The virtual invisibility of phylogeny in textbooks was finally

ended by Dobzhansky et al. (1977), who included a

short discussion of numerical taxonomy and cladistics, several

phylogenies illustrating macroevolutionary histories such

as the origin of amphibians, several phylogenies based on

distance analyses of molecular data (including some of Ayala’s

own work with electrophoresis), and perhaps most interesting,

an illustration of how a phylogeny of Hawaiian Drosophila,

based on chromosome inversions, supported a

postulated history of interisland colonization. This example

suggested that phylogenies could be useful for evaluating

hypotheses about evolutionary histories. The first edition of

my own textbook (Futuyma 1979) described phenetic and

cladistic methods, included several phylogenies illustrating

the history of diversification, presented several phylogenies

as a basis for hypotheses about evolutionary processes

(fig. 3.1), and emphasized that “all the examples of rates and

directions of evolutionary change discussed [are based] on

the assumption that it is possible to infer the phylogenetic

history of species correctly.”

The resurgence of phylogenetic research and its slow

integration into the broader field of evolutionary studies, as

reflected by these textbooks, had several causes. First and

foremost were attempts to develop rigorous, quantitative

methods for erecting classifications (Sokal and Michener

1958) and especially for inferring phylogenies (e.g., Hennig

1950, Edwards and Cavalli-Sforza 1964, Kluge and Farris

1969, Felsenstein 1973). The expectation of greater rigor

made the phylogenetic enterprise more optimistic, more

conceptually dynamic, and thus more attractive to prospective

researchers in the field, and made it potentially more

respectable in the view of evolutionary biologists outside the

field. [However, I suspect the integration of phylogenetic

The Fruit of the Tree of Life 27

systematics and other fields of evolutionary study would have

happened faster if nonsystematists had not recoiled from the

“warfare” among adherents to different systematic doctrines

(Hull 1988) and from the astonishingly combative language

and behavior of some partisans.]

Second, phylogenetic study became supported by new

kinds of data and pursued by individuals trained in a different

tradition. Molecular data enabled individuals to do phylogenetic

study without apprenticeship in taxon-specific

comparative morphology, especially if a molecular clock were

valid. Moreover, such data, especially amino acid sequences

and electrophoretic allele frequencies, could be interpreted

from the perspective not only of systematics but also from

that of population genetics. The contributions of individuals

whose work embraced both populations genetics and

phylogeny (e.g., Felsenstein, Nei, Templeton) may have met

resistance from organism-oriented systematists (and to some

extent still do), but they did and do form a bridge between

phylogenetics and process-oriented evolutionary biology.

Third, the 1970s saw a resurgence of interest in macroevolution,

including topics such as developmental constraints

(and “evo-devo” generally), punctuated equilibrium

and its proposed implication for evolutionary trends, species

selection and the differential diversification of clades, and

changes in diversity through the Phanerozoic. Such topics

could hardly be studied without a phylogenetic framework.

Fourth, some individuals urged a synthesis between

phylogenetics and studies of evolutionary processes, and

undertook research that required such synthesis. Almost

from its inception, the study of molecular evolution depended

on a phylogenetic framework, as in the revelation and

analysis of gene duplication (e.g., Goodman et al. 1982) and

in tests of rate constancy in sequence evolution (Wilson et al.

1977, Kimura 1983). Some systematists (especially young

ones) eagerly sought ways of applying phylogenetic methods

to evolutionary questions in areas such as coevolution

and character evolution (Brooks and Glen 1982, Mitter and

Brooks 1983, Sillйn-Tullberg 1988). Felsenstein (1985) offered

a method of accounting for phylogeny in comparative

studies of adaptation in a paper that elicited more reprint

requests than anything else he had published (J. Felsenstein,

pers. comm.). In a 1987 address to the Society for the Study

of Evolution (SSE), I described ways in which phylogenetic

and process-oriented studies could inform each other

(Futuyma 1988); later, I organized a symposium on this

theme for the 1988 meeting [several of the talks were published

in Evolution 43(6):1137–1208].

A synthesis slowly developed despite extraordinary Sturm

und Drang (“storm and stress”) in the late 1970s and early

1980s, when it seemed as if “macroevolutionists” and

“microevolutionists” were forming increasingly isolated, even

hostile, camps (Futuyma 1988). At meetings of the SSE from

1981 through 1988, only about 4% of contributed papers

referred to phylogeny (judging from titles in the programs),

but this increased to 12% in 1989, when the meeting also

included symposia on phylogenies based on ribosomal genes

(organized by E. Zimmer and D. Hillis) and on cladistic approaches

to evolutionary innovation (organized by C. Mitter

and B. Farrell). In 1990, the SSE met with other societies in

the fifth International Congress of Systematic and Evolutionary

Biology, the theme of which (“the unity of evolutionary

biology”) was conceived explicitly as a synthesis of historical

and process-oriented evolutionary disciplines (C. Mitter,

pers. comm.). At this meeting, the Society of Systematic

Zoologists decided to become the Society of Systematic Biologists

and to meet jointly with the SSE thereafter (Hillis

2001). The joint meetings now include both symposia and a

high proportion (about 26% in 2001) of contributed papers

with a phylogenetic theme or flavor. Many of the papers

explicitly apply phylogenetic methods or information to a

wide variety of problems in evolutionary biology. Of course,

this growing mutualism between phylogenetic systematics

and other subdisciplines of evolutionary biology has also

become evident in the contemporary literature.

Phylogenies in Contemporary Evolutionary

Biology and Ecology

In the mid-1980s, phylogeny was almost invisible in the

pages of Evolution and of most other evolutionary journals.

Less than two decades later, it pervades the literature on almost

every major subject in evolution, to the point at which

some have wondered if demands for a phylogenetic framework

may even be sometimes excessive (e.g., Westoby et al.

1995; see Silvertown et al. 1997). Moreover, we now seek

phylogenies not only of species and higher taxa, but also of

Figure 3.1. A rare, early example of a phylogenetic tree used

to exemplify an important evolutionary principle. L. H.

Throckmorton illustrated parallel evolution of the form of the

male ejaculatory bulb in species of the Drosophila repleta species

group, displaying the morphology on a phylogeny inferred from

chromosome inversions. After Throckmorton (1965) and

Futuyma (1979).

28 The Importance of Knowing the Tree of Life

genes within genomes and of variant gene sequences within

and among species. The same methods can yield trees for

organisms and trees for genes, which in turn can shed light

on the history and processes that have affected genomes,

organisms, and populations.

The many issues in evolution and ecology that are informed

by phylogenetic analysis (table 3.1) fall under several

major headings, each of which I address briefly below

with a few examples. My emphasis is on questions pertaining

to the evolution and ecology of organisms and thus,

chiefly, on rather traditional questions that phylogenetics can

now help answer. I will not treat molecular evolution, in

which phylogenetic analysis bears on almost every topic, such

as rates of sequence evolution, mutation, and recombination;

the evolution of gene families and the homology (paralogy)

of functionally different genes; horizontal gene transfer; the

time of silencing of pseudogenes; and many others. These

topics warrant book-length treatment (e.g., Li 1997) and are

far from my areas of competence.

Evolutionary Processes within Species

Phylogenetic methods provide insights into evolutionary processes

within species by way of both phylogenies of genes and

phylogenies of populations and species. Traditional population

genetic theory deals with the ways in which frequencies of

alleles are affected by mutation, genetic drift, gene flow, and

natural selection. Coalescent theory expands traditional population

genetic theory by analyzing these processes in a history

of phylogenetic (or genealogical) relationships among the alleles

(Hudson 1990). For example, a population with a constant

size of Ne breeding individuals may begin with different

gene lineages, each of which diversifies as new mutations occur.

If all the sequences are selectively equivalent (neutral), gene

lineages become extinct by genetic drift, at a rate inversely

proportional to the population size. After about 4Ne generations,

all except one original lineage will have become extinct,

on average, such that all genes are descended from (“coalesce

to”) one of the original genes. What began as a genetically

“polyphyletic” population becomes monophyletic because of

genetic drift. The gene tree continues to branch by mutation,

but because the tree is continually pruned by genetic drift, only

a large population will contain multiple old (“deep”) branches

that differ by many mutations. Therefore, a gene tree with deep

branches indicates a population that has been large or subdivided,

and a shallow gene tree signals a small or bottlenecked

population (assuming selective neutrality). Given an estimate

of the mutation rate (u), in fact, the effective population size

can be estimated from the frequency of heterozygotes per site

(which is expected to equal the product 4Neu at a diploid

locus).

The gene tree can also be affected by selection. For example,

balancing selection can maintain different gene lineages,

giving rise to much deeper branches in the gene tree

than expected from Ne alone, whereas directional selection

that recently fixed an advantageous mutation will have swept

away linked neutral variation, resulting in a very shallow gene

tree (of sequences that have arisen by mutation since the

selective sweep). The effects of selection versus genetic drift

can be distinguished by comparing multiple genes that are

not closely linked, because genetic drift affects all genes similarly

whereas selection affects genes individually.

Among the best-known applications of this approach to

date are analyses of human gene trees, which fairly consistently

imply that the effective size of the human population

has been quite small, on the order of 100,000 or less. (The

effective size, which is approximately the harmonic mean

of breeding numbers in successive generations, is mostly

strongly determined by reductions, or bottlenecks, in size.

Therefore, the recent explosive growth of the human population

has had little effect on Ne.) Although many basal gene

lineages are found in African populations, almost all non-

African haplotypes belong to a single nonbasal clade—points

that strongly favor the hypothesis that the contemporary

human population of the world has been derived from an

African population in the very recent past (e.g., Hammer

1995, Ingman et al. 2000). This approach to estimating historical

effective population size might also be applied to

historical bottlenecks that may have accompanied speciation.

In such a study of a pair of sister species of leaf beetles

(Ophraella), we estimated that Ne was greater than one million,

a far cry from a bottleneck (Knowles et al. 1999). However,

there may have been enough time since speciation of

these beetles for high sequence variation to have been regenerated

even if there had been a bottleneck; the method will

detect a bottleneck only if divergence has been too recent for

coalescence to have occurred in a large population. Similar

analyses do indicate small Ne, perhaps due to a speciation

bottleneck, in Drosophila sechellia, endemic to the Seychelles

Islands (Kliman et al. 2000).

In contrast to the very shallow branches of most human

gene genealogies, the tree for human genes in the major histocompatibility

complex (MHC) shows very deep branches;

in fact, different human haplotypes are more closely related

to chimpanzee MHC haplotypes than to other human haplotypes.

Thus, the MHC polymorphism has been maintained

for more than 5 million years, longer than expected for neutral

variants if current estimates of human Ne are correct. The

gene tree thus provides prima facie evidence of balancing

selection. It has been suggested that selection by diverse

parasites may have maintained variation (Hughes 1999).

Probably the most active area of research in intraspecific

phylogeny is phylogeography, the study of the geographic

distribution of genealogical lineages (Avise 2000). Often combined

with coalescent analysis, such studies are shedding

light on histories of population subdivision, gene flow, colonization,

and range expansion. For example, the classic studies

of Bermingham and Avise (1986) revealed a common

history of vicariant differentiation in several species of freshThe

Fruit of the Tree of Life 29

water fishes in the southeastern United States: The mitochondrial

gene tree of each species included two major clades of

variant sequences, distributed to the west and east of a probable

Pliocene saltwater barrier. Similar studies have revealed

the likely sites of refugia for many species during Pleistocene

glacial episodes and the routes of postglacial colonization

(e.g., Taberlet et al. 1998). Postglacial expansion over broad

areas by relatively few colonists appears now to account for

lower levels of genetic variation within and among populations

at higher latitudes than at lower latitudes. For example,

northern populations of MacGillivray’s warbler (Oporornis

tolmiei) collectively have a shallower mitochondrial gene tree

than do southern populations (fig. 3.2; Milб et al. 2000).

Phylogenies of species rather than genes can also help to

illuminate evolutionary processes. For example, the relative

rate test for constancy of sequence evolution requires phylogenies,

and approximate constancy, together with timecalibrated

divergence between taxa, is the basis of most

estimates of mutation rates at the molecular level (Kimura

1983). A very different example is provided by studies of

sexual selection. For instance, Basolo (1996) found that in

fishes of the genus Xiphophorus, females prefer males with a

Table 3.1

Some Applications of Phylogenetic Study in Evolutionary Biology and Ecology.

I. Evolutionary processes within species

1. Isolation, vicariance, and gene flow Avise (2000), Zink et al. (2000)

2. Colonization and range expansion Taberlet et al. (1998), Ballard and Sytsma (2000)

3. History of population size Takahata et al. (1995), Wakeley and Hey (1997)

4. Mutation rates Kimura (1983), Lynch et al. (1999)

5. Selection on DNA sequences Hudson (1990)

6. Sexual selection Basolo (1996), Barraclough et al. (1995)

7. Asexual reproduction vs. recombination Guttman and Dykhuizen (1994)

II. Character evolution

1. Meaning and identification of homology and homoplasy Sanderson and Hufford (1996), Wagner (1989)

2. Rates of evolution Lynch (1990), Gittleman et al. (1996)

3. Inferring lability and constraint Gittleman et al. (1996)

4. Comparative method of inferring adaptation Felsenstein (1985), Martins (1996)

5. Polarity, evolutionary sequences, origin of novelties Donoghue (1989), Lee and Shine (1998), Wahlberg (2001)

6. Genome evolution (duplications, repeated sequences, etc.) Fitch (1996), International Human Genome Sequencing Consortium

(2001)

7. Locating candidate genes for traits Crandall and Templeton (1996)

8. Historical framework for experimental analyses Futuyma et al. (1995), Ryan and Rand (1993)

III. Speciation

1. Delimiting species Avise and Ball (1990), Baum and Shaw (1995)

2. Geographic pattern of speciation Schliewen et al. (1994), Berlocher (1998), Barraclough and Vogler

(2000), Coyne and Price (2000)

3. Demography of speciation Knowles et al. (1999), Hare et al. (2002)

4. Duration of speciation process McCune and Lovejoy (1998), Avise and Walker (1998)

5. Hybrid speciation, introgression Rieseberg (1997), Dowling and Secor (1997)

6. Pattern of evolution of reproductive isolation Coyne and Orr (1989)

7. Dating speciation Klicka and Zink (1997), Knowles (2000)

IV. Diversity

1. Hypotheses for diversification (e.g., key adaptations) Mitter et al. (1988), Sanderson and Donoghue (1996)

2. Estimating speciation and extinction rates Mooers and Heard (1997), Barraclough and Nee (2001)

3. Estimating number of ghost lineages Sidor and Hopson (1998)

4. Cospeciation of interacting lineages Brooks and McLennan (1991), Page and Hafner (1996)

5. Adaptive radiation Givnish and Sytsma (1997), Schluter (2000)

6. Hypotheses for regional diversity differences Qian and Ricklefs (1999), Chown and Gaston (2000)

V. Ecology

1. Community assembly: geographic sources of species McPeek (1995), Zink et al. (2000)

2. Community assembly: evolution of interactions Farrell and Mitter (1993), Futuyma and Mitter (1996)

3. Coexistence in relation to phylogenetic affinity Webb (2000)

4. Convergence in community structure Losos et al. (1998)

5. Changes in viral infection rates Holmes et al. (1996)

VI. Conservation

1. Identifying “management units” and “evolutionarily Vane-Wright et al. (1991), Moritz (1994)

significant units”

2. Conserving “evolutionary history” Purvis et al. (2000a)

3. Predicting extinction risk Purvis et al. (2000b)

30 The Importance of Knowing the Tree of Life

sword (an elongation of the lower caudal fin rays). Remarkably,

females display such a preference not only in those

species that have swords (swordtails) but also in species that

normally lack them (platies). Although different estimates of

phylogenetic relationships within Xiphophorus made it ambiguous

whether or not the female preference in swordless

species reflected a plesiomorphic state (i.e., preference having

evolved before the male sword), Basolo showed that the

female bias also characterizes Priapella, an indisputably primitively

swordless sister lineage of Xiphophorus. At the time, the

idea that preexisting female preferences may play a role in

sexual selection was a rather new hypothesis, contending

with several other models of sexual selection by female

choice.

Speciation

Studies of speciation must have an intimate relation to phylogeny,

if for no other reason (obvious now, but perhaps not

always so) than that it is often necessary to identify correctly

the products of a speciation event, namely, sister species.

Even the delimitation of species may depend on phylogenetic

data, at least for those who prefer to define species in genealogical

terms, such as genetic monophyly (e.g., Baum and

Shaw 1995; see also Avise and Ball 1990). A phylogeny is a

sine qua non for identifying instances in which new species

have arisen from interspecific hybrids (e.g., Rieseberg 1997)

and for dating speciation events. For example, successive

speciation events have apparently occurred within the Pleistocene

in montane Melanoplus grasshoppers (Knowles 2000).

In contrast, many sister species of North American birds that

were formerly presumed to have arisen in Pleistocene glacial

refugia appear to have diverged in the Pliocene (Klicka and

Zink 1997), although speciation is a continuing process that

in some of these cases probably extended into the Pleistocene.

This conclusion arises from the suggestion that the minimal

duration of the speciation process may be estimated from the

difference between the temporal depth of the branch point

between sister species and the temporal depth of the deepest

nodes within the gene tree of one of those species

(McCune and Lovejoy 1998, Avise and Walker 1998). On

this basis, Avise and Walker (1998) concluded that speciation

in birds and mammals generally takes about 2 Myr (million

years), so populations that began diverging in the later

Pliocene would have completed speciation in the Pleistocene.

McCune and Lovejoy (1998) used this approach to compare

the estimated duration of speciation in clades in which allopatric

speciation is probable and clades in which they considered

sympatric speciation a likely possibility. The results

of their analysis were consistent with the hypothesis that

sympatric speciation, which cannot occur except by strong

selection, should be faster than allopatric speciation.

How to distinguish sympatric from allopatric speciation,

and even how to provide convincing evidence that sympatric

speciation occurs, have long been vexing questions. Phylogenetic

approaches are at last promising answers. Probably

the most convincing case of completed sympatric speciation

is provided by several apparently monophyletic species

groups of cichlids in crater lakes in Cameroon (Schliewen

et al. 1994). The lakes are structurally simple and ecologically

rather homogeneous, so if speciation occurred within

the lakes, as the phylogeny implies, it must have been truly

sympatric. In birds, in contrast, monophyletic species groups

have evidently not evolved on islands that lack topographic

and vegetational barriers, suggesting that bird speciation is

Figure 3.2. An example of

inference of historical demography

in a phylogeographic analysis.

Samples of a mitochondrial

cytochrome gene in MacGillivray’s

warbler (Oporornis tolmiei) from

localities in western United States

and a small region in northern

Mexico show high haplotype

sequence diversity in Mexico,

whereas the northern samples

include only a single common

haplotype and rare, presumably

recently originated variants that

differ from the common haplotype

by single mutations. The gene tree

(or network) is consistent with the

hypothesis that northern populations

are derived from relatively

small numbers of postglacial

founders. After Milб et al. (2000).

(a) (b)

1, 2, 3, 4, 5, 6, 7, 8

9, 10, 11, 12, 13

1, 2

11

2, 3

7

7, 9

10

13

14

14

14 14

13, 14 13 13, 14

14 14

11

12

10

1

9

6 8 7

2

3

4

5

2, 7

7

13, 14

13, 14

The Fruit of the Tree of Life 31

usually allopatric, as has long been thought (Coyne and Price

2000). In another approach to the problem, suggested by

Berlocher (1998) and Barraclough and Vogler (2000), the

degree of range overlap between sister taxa in a clade is plotted

against a surrogate for divergence time (e.g., sequence

divergence). The overlap between sympatrically originated

taxa must remain high or decline (because they start with

maximal overlap of the smaller range by the larger), whereas

overlap between the ranges of allopatrically originated taxa

can only increase with time. Most of the phylogenies analyzed

by Barraclough and Vogler (2000) were consistent with

allopatric speciation, but two insect phylogenies suggest a

role for sympatric speciation.

Character Evolution

Probably all claims about the evolution of characters among

species must have a phylogenetic foundation. Historically,

this was often not explicitly stated or perhaps even recognized,

but clearly phylogenetic assumptions underlie the

belief that parasites have “degenerated” in morphology, or

that Hyracotherium and subsequent equids represent a transformation

series. Today, phylogenies are the explicit basis for

many, perhaps most, studies of character evolution, whether

phenotypic or molecular. They are required to distinguish

homology from homoplasy and to estimate rates of character

evolution. “Conservative” characters, with low evolutionary

rates, provide material for analysis of possible constraints.

Homoplasy provides data for the analysis of adaptation by

the “comparative method” (Harvey and Pagel 1991), which

most practitioners now agree should be based on explicit

phylogenies, so that independent evolutionary changes in a

trait of interest can be correlated with environmental factors

or with other characters.

Phylogeny has long been the (at least implicit) basis for

understanding character transformations, such as the origin

of novel features (e.g., wings, auditory ossicles, the sting of

aculeate Hymenoptera). This enterprise is being rejuvenated

as the developmental and genetic bases of such transformations

are illuminated in a phylogenetic framework. Both conservation

and change in the expression and functional roles

of Hox genes, for example, provide unprecedented insights

into evolutionary changes in body plans (Carroll et al. 2001).

We are also better able to evaluate traditional ideas about the

polarity of character evolution. For example, the venerable

idea that ecological specialists evolve from generalists far

more often than the converse has many implications; it might

explain, in part, why many clades of herbivorous insects are

composed mostly of host-specialized species (Futuyma and

Moreno 1988). Only recently, however, has breadth of resource

use been mapped onto phylogenies in order to infer

the direction of change. In some cases, such as the host range

of Dendroctonus bark beetles, the traditional hypothesis has

been supported (Kelley and Farrell 1998). In quite a few other

phylogenies, however, at least some generalists arise from

more specialized ancestors (Nosil 2002), and although it may

be premature to conclude that there is “little support for the

generalist-to-specialist hypothesis” (Schluter 2000), it is certainly

clear that any such trend is far from universal.

To an increasing extent, even experimental studies of

character evolution are being designed in a phylogenetic or

historical framework. For example, I explicitly conceived my

own work on host shifts in Ophraella (Coleoptera: Chrysomelidae)

as a study of a character that systematics had shown

to be interesting, and as an example of mutualism between

phylogenetic and population genetic approaches. Insect systematists

have long known that host–plant association is a

highly conservative character in many groups of phytophagous

insects; clades that may date back to the Cretaceous

often are restricted to a single plant family (Ehrlich and Raven

1964, Farrell and Mitter 1993). Such features invite the

hypothesis that internal constraints may limit evolution

(Maynard Smith et al. 1985). Such constraints might manifest

by absence or paucity of genetic variation (the prerequisite

for any evolution). I posed the hypothesis that the pathways

of evolution of host affiliation actually taken by an insect clade

may have been more likely, because of constraints on some

characters rather than others, than the paths not taken

(Futuyma et al. 1993, 1995). Thus, for example, if most host

shifts have been between closely related rather than distantly

related plants, this hypothesis predicts that features necessary

for survival and reproduction on a novel plant would

be more genetically variable if the plant is closely related than

if it is distantly related to the insect’s current host plant.

Most of the 14 currently recognized species of Ophraella

feed only on one or another genus of plant, in one of four

tribes of Asteraceae. Our proposed phylogeny of Ophraella,

based first on morphological and allozyme characters and

later on mitochondrial gene sequences (fig. 3.3; Funk et al.

1995), provides no evidence for cospeciation or codiversification

with the host plants but does show that host shifts

have been more frequent within than between host tribes

(i.e., adaptation to closely related plants has been the norm).

Larval and adult beetles feed and survive much better on their

own hosts than on those of their congeners, and in some

instances the (presumably chemical) barriers to feeding result

in almost no feeding at all. Using breeding designs commonly

employed in quantitative genetics, we screened large

numbers of naive hatchling larvae and newly eclosed adults

for their feeding response to and ability to survive on foliage

of as many as six species of plants that are hosts of Ophraella

species, but not of the particular species being screened. We

performed such screens for genetic variation in feeding response

and survival with four species of Ophraella, resulting

in a total of 18 combinations of insect and plant species

screened for genetic variation in survival and 39 screens

of feeding responses (including both larval and adult responses).

Overall, we detected genetic variation in survival

in only two cases: in both, the plant that supported geneti32

The Importance of Knowing the Tree of Life

cally variable survival was very closely related (in the same

subtribe) to the beetle species’ normal host. Although the

correlation was not strong, genetic variation in feeding response

was significantly more frequent among tests of species

on closely related plants (in the same tribe as the normal

host) than on distantly related plants (in a different tribe of

the Asteraceae). The results are consistent with the hypothesis

that a macroevolutionary pattern of host association revealed

by phylogenetic analysis may stem in part from genetic

biases revealed by the methods of evolutionary genetics.

Diversity

It seems hardly possible to discuss the origin of organismal

diversity without reference to phylogeny. For example, textbook

treatments of the subject have usually included phylogenetic

diagrams (frequently including reference to

stratigraphic distributions, as in classical portrayals of the

history of the Equidae). It is only recently, however, that

phylogenies have served as explicit tools for testing hypotheses

about the history and causes of diversification. For example,

parasitologists had proposed phylogenetic hypotheses

about parasite–host associations by the 1940s, but only in

the early 1980s were phylogenies explicitly used to determine

whether the associations were caused by cospeciation and

codiversification (one form of coevolution) or by lateral shifts

of parasites among preexisting lineages of hosts (e.g., Brooks

and Glen 1982, Mitter and Brooks 1983). Subsequent research,

including development of methods for distinguishing

these hypotheses, has made it clear that different groups

of parasites and symbionts (sensu lato, including phytophagous

insects, microbes, etc.) exemplify both historical patterns

(Page and Hafner 1996).

Phylogenies provide by far the most important basis for

testing hypotheses about the role of “key innovations” as

causes of differences in rates of diversification among clades.

The tradition of attributing the high diversity of insects to

the evolution of wings, or of Coleoptera to elytra, or of angiosperms

to the carpel has been criticized as ad hoc,

untestable “storytelling,” because each such event is unique

(lacking the replication required for any statement about

correlation), and each could in principle be attributed to any

of the many other apomorphies of these groups (even assuming

that their diversity has indeed been caused by any such

character). The method of replicated sister-group comparisons

introduced by Mitter et al. (1988) provides a more rigorous

test by comparing the species diversity of multiple

clades in which a putative diversity-enhancing character has

independently originated with that of their sister groups that

lack the character. The use of sister groups enables diversity

differences to be ascribed to differences in rate of speciation

and/or extinction rather than differences in age, and the replication

provides a basis for statistical test. Mitter et al. (1988)

provided evidence that acquisition of the habit of herbivory

has enhanced the rate of insect diversification, and Farrell

(1998) later used this approach to argue that diversification

rate in phytophagous beetles has been greatly increased by

shifts from “gymnosperm” to angiosperm hosts. The hypothesis

that plant diversification has been enhanced by the evolu-

Figure 3.3. The phylogeny of species of Ophraella leaf beetles, connected by arrows to their host

plants. The hosts belong to four tribes of Asteraceae, indicated by different shading. The poor

congruence between the trees is consistent with other evidence that the beetles have shifted

among host lineages, for the most part, rather than cospeciating with their host plants. Host shifts

have been more frequent within than between plant tribes, illustrating conservatism of diet. The

beetle phylogeny is based on mitochondrial DNA sequences, and that of the plants on chloroplast

DNA studies (see Funk et al. 1995). A complete plant phylogeny would include many other

intercalated genera and tribes. From Futuyma and Mitter (1996).

The Fruit of the Tree of Life 33

tion of defenses against herbivores—a key element of Ehrlich

and Raven’s (1964) scenario of coevolution—was supported

by the consistently greater species diversity of plant lineages

with latex or resin canals in sister-group comparisons—features

that have been experimentally shown to deter insect

herbivores (fig. 3.4; Farrell et al. 1991). Both key innovations

and ecological opportunity offered by “empty ecological

space” are associated with enhanced diversification rate, as

the many phylogenetic studies of adaptive radiation are demonstrating

(Givnish and Sytsma 1997, Schluter 2000).

Differences in species diversity among geographic regions

and among environments have attracted attention from both

ecologists and evolutionary biologists. Latitudinal gradients in

diversity, for example, might represent equilibrial conditions

dictated by interactions among species, or might have a more

historical explanation based on the history of speciation and

extinction (Chown and Gaston 2000). Stebbins (1974), for

example, suggested that the tropics might be a “cradle” of new

species originating at higher rates than elsewhere, or a “museum”

in which extinction rates have been low and species have

accumulated over vast spans of time. Phylogenies that provide

time depths for many of the clades that contribute to the diversity

differences will probably play an important role in resolving

this long-persistent controversy. For example, a

molecular phylogenetic study of the diverse neotropical tree

genus Inga (Fabaceae) suggests that most of the approximately

300 species have originated within the last 6 Myr, favoring the

“cradle” interpretation (Richardson et al. 2001). On the other

hand, diversity at the level of higher taxa (genera, families) may

also be highest in tropical latitudes, suggesting that much more

comprehensive phylogenies will be needed to compare the distribution

of divergence times that would account for differences

in diversity between regions.

Geographical variation in species diversity and taxic composition

stems in part from the processes that are the subject

of historical biogeography (Morrone and Crisci 1995,

Humphries and Parenti 1999). This field has always been

inseparable from phylogenetic systematics, because the

higher taxa that are its subject must have phylogenetic meaning.

Part of the “cladistic revolution,” in fact, consisted of

attempts to establish a more rigorous phylogenetic framework

to analyze distributions, in the form of “vicariance biogeography”

(Nelson and Platnick 1981). The null hypothesis

or guiding principle was that distributions of taxa should be

explained by successive disjunctions among regions or areas,

resulting in congruent cladograms of taxa and of the areas

they occupy. However, the disparagement of “dispersalist”

explanations by some early vicariance biogeographers has

proven unwarranted, for phylogenetic analyses have been

equally powerful in providing evidence of dispersal. For example,

a recent analysis of the Chamaeleonidae, based on 644

parsimony-informative molecular, morphological, and behavioral

characters, provides strong evidence that chameleons

originated in Madagascar after its separation from India,

and later dispersed to Africa (at least twice), the Seychelles,

and the Comoros archipelago (fig. 3.5; Raxworthy et al. 2002).

Chameleons are among many taxa distributed around the

Indian Ocean that show more phylogenetic evidence of dispersal

than of the Gondwanan vicariance that might have

been expected. As more phylogenies are developed, a balanced

view of the roles of vicariance and dispersal is emerging

(Zink et al. 2000).

Community Ecology

The problems addressed by community ecology include the

species diversity and composition of species assemblages, and

the structure of their interactions (e.g., food web structure).

An evolutionary perspective has been important in community

ecology, both by suggesting how evolutionary responses

to interspecific interactions may shape community character

and by emphasizing the effects of history.

That community composition and structure may be affected

by “deep” evolutionary history should be a clear lesson

from historical biogeography. The absence of mammals

from New Zealand, of sea snakes from the tropical Atlantic,

and of bromeliads from Old World tropical forests must

count as major differences in community structure, even if a

Figure 3.4. Replicated sister-group contrasts can test for effects

of apomorphic characters on diversity. These are two of the

sister-group pairs of seed plants in which species richness is

higher in the clade with apomorphic latex- or resin-bearing

canals. Based on Farrell et al. (1991).

Figure 3.5. A reduced phylogeny of lineages of

Chamaeleonidae, showing the pattern of distribution in

Madagascar (M), Africa (AF), India (I), and the Seychelles (SE).

The phylogeny supports the hypothesis of dispersal from

Madagascar and is incompatible with postulated histories of the

separation of these land masses. After Raxworthy et al. (2002).

34 The Importance of Knowing the Tree of Life

few species play faintly convergent roles (moas, e.g., being

possible ungulate vicars). Thirty years ago, the discourse of

community ecology made little reference to historical accident,

because of a conviction that rapid evolutionary responses to

strong ecological interactions should have almost deterministically

shaped predictable equilibrial structures. This conviction,

or faith, has been shaken, and community ecologists now

appear to have a growing appreciation of the importance of

history. For example, plant species that we think of as forming

coherent assemblages (e.g., maple and hemlock) seem to

have undergone quite independent shifts in distribution

throughout the Pleistocene (Davis 1976), and differences in

the species diversity of trees in Europe, eastern Asia, and eastern

North America appear largely attributable to differences

in extinctions suffered during glacial episodes, owing to differences

in the availability of temperate refuges (Latham and

Ricklefs 1993, Qian and Ricklefs 1999).

The impact of much older evolutionary histories has been

little analyzed but must be equally significant. For example,

many clades of phytophagous insects are so conservative in diet

that they have remained associated with the same plant family

since the early Cenozoic or earlier (Farrell and Mitter 1993,

Farrell 1998). Many genera of leaf beetles (Chrysomelidae) that

in New York State feed on only a single plant family include

other species that also exist in western North America, Europe,

or tropical America. In almost every case, the congeners in

those biogeographic regions feed, exclusively or in part, on

the same plant families as do their New York relatives (table

3.2; Futuyma and Mitter 1996). Thus, the producer–consumer

interface in communities in New York represented by

these insect–plant associations must have been shaped in part

by sorting among colonizing species from other regions, whose

establishment depended on host-related characters that had

evolved many millions of years before. (We cannot confidently

specify the direction of colonization for most of these genera,

because the required phylogenies have not been determined—

one example among many in which a more complete Tree of

Life would help to describe ecological history.)

The processes that give rise to an assemblage of stably

coexisting species include both sorting among colonists from

a regional species pool and evolutionary (or coevolutionary)

responses to species interactions in situ. That is, the characteristics

that enable species to coexist may have been “preadaptations”

that evolved before they came into contact or

may have evolved in response to the interaction between

them. These processes (which are not mutually exclusive)

have been difficult to distinguish, but phylogenetic approaches

are providing some resolution. For example, islands

in the Lesser Antilles harbor either one species of anole, usually

of medium body size, or two species, usually a small and

a large one. (Differences in body size are correlated with differences

in average prey size, and thus facilitate coexistence.)

Although this pattern suggests repeated character displacement

between competing species on two-species islands, a

phylogeny of the species suggests that the three small species

form a monophyletic group and that the two large species

that occur on two-species islands likewise are a monophyletic

group (Losos 1992). Thus, even if character displacement

occurred once, several two-species islands must have been

colonized by lineages that already differed in body size, conforming

to the hypothesis that preexisting ecological differences

are required for species to come into coexistence.

Moreover, the independent evolution of large size in one

species (A. ferreus) on a one-species island suggests that character

displacement may not be the sole explanation for evolutionary

changes in size.

In contrast to the Lesser Antilles, where coexistence of

ecologically different species has been due mostly to species

sorting, the Greater Antilles harbor four monophyletic groups

of anoles that have undergone strikingly similar adaptive

radiations (Losos 1992, Losos et al. 1998). “Ecomorphs” that

differ in size, shape, and microhabitat use have evolved in

parallel in Cuba, Hispaniola, Jamaica, and Puerto Rico (although

the set is slightly incomplete on the latter two islands).

It is likely that character displacement among competing

species has caused the adaptive divergence. The phylogenetic

framework is crucial for showing that the community structure

on the several islands has arisen not by sorting ecologically

dissimilar from similar species (as in the Lesser Antilles)

but by selection stemming from species interactions and the

intrinsic functional relationships between anoles and their

resources. The belief in predictable evolution of community

structure may not be entirely groundless.

Phylogenetic data may also cast light on the processes that

affect species assemblages on short time scales (i.e., in ecological

time). For example, hypotheses accounting for the

high species diversity of trees in many tropical forests include

neutral “drift” in the frequencies of ecologically equivalent

species (the number of which is ultimately determined by

long-term rates of speciation and extinction; Hubbell 2001);

greater herbivore- or pathogen-induced mortality of conspecific

than allospecific seedlings in the neighborhood of adult

trees, resulting in underdispersion of each species (Janzen

1970, Connell 1971); and “niche partitioning” among species,

based in part on use of different microhabitats. Webb

(2000) reported that tree species within 0.16–hectare plots

Table 3.2

Fraction (p) of New York Genera of Chrysomelidae

(Numbering n) that Share at Least One Host Plant Family

with Congeners in Europe and Tropical America.

Number of host families in New York

1 2 3 or more

p n p n p n

Europe 0.94 16 1.00 9 0.97 29

Tropical America 0.93 14 1.00 8 0.80 5

After Futuyma and Mitter (1996).

The Fruit of the Tree of Life 35

in lowland dipterocarp forest in West Kalimantan, Indonesia,

were phylogenetically closer, on average, than if they had

been drawn at random from the entire local pool of 324 species.

This pattern is consistent with the hypotheses that phylogenetic

affinity is correlated with ecological similarity and that

the overall species diversity consists, in part, of assemblages

of related species in a mosaic of different microhabitats.

Practical Applications

So many applications of biology depend on taxonomy that

we are inclined to forget that phylogenetic assumptions

underlie the applications. For instance, a major method of

weed management is the use of biological control agents, such

as host-specific insects that might be imported from the

weed’s region of origin. The bulk of research on such insects

consists of tests to assure that they will not attack economically

important plants such as crops. Most of this effort is

devoted to tests of responses to plants in the same higher

taxon as the weed, that is, closely related plants. It may seem

obvious that a control agent for a weedy species of thistle

might be a potential threat to artichoke crops (a member of

the same tribe), but of course this rests on an assumption of

a phylogenetically sound classification. Conservation biologists

have recently raised the concern that biological control

agents may attack threatened native species; for example, the

weevil Rhinocyllus conicus was introduced to North America

from Europe to control several adventitious European

thistles, but it also attacks several native thistles (Louda et al.

1997). (Advocates of biological control counter criticism by

saying that such spread was expected, but that concern for

native plant species was not a criterion for introduction when

the Rhinocyllus program was implemented.) I have suggested

that screening of potential biological control include tests for

genetic variation in the species’ fitness on closely related

nontarget species, because genetic adaptation to closely related

plants is a common pattern in many clades of herbivorous

insects (Futuyma 2000).

Several authors have urged that phylogenetic information

be brought to bear in conservation biology (e.g., Vane-

Wright et al. 1991, Moritz 1994, Purvis 2000a, 2000b). One

might consider giving priority to conserving “phylogenetic

history,” if, for instance, the choice lay between a species flock

of very closely related species and an ecosystem that included

endemic or species-poor long phylogenetic branches (e.g.,

Sphenodon, Welwitschia). Phylogenetic or phylogeographic

information may likewise help to identify “evolutionarily significant

units” for management (Moritz 1994).

Conclusions

In an astonishingly short time, phylogenetic methods or

frameworks have become integral parts of almost every major

area of evolutionary biology, and several parts of ecology

as well. A steady stream of papers suggests new uses for

phylogenies, with no end of inventiveness in sight. Because

it is clear that phylogenetic approaches and data will play an

increasingly important role in biological disciplines outside

systematics, we might ask how the mutualism between phylogenetic

systematics and the other “biodiversity sciences” might

best be fostered. I do not presume to offer a deep or even wellinformed

analysis, but instead a few modest suggestions.

First, systematists and the users of systematics might do

well (even for utterly self-serving reasons) to engage in some

of their work with an eye toward their mutual or reciprocal

benefit. For instance, ecologists engaged in biological inventory

projects amass collections that may include huge numbers

of species, many rare or even undescribed. The value of

these collections for phylogenetic purposes would be enormous

if some specimens (or tissues) of each species were

cryopreserved for future molecular study. Systematists who

are engaged to help identify material from such inventories

might consider how future phylogenetic studies of both their

“own” taxa and others might be aided if they were to insist

that comprehensive samples be donated to frozen tissue

collections.

The fruits of phylogenetic studies will be most bountiful

if they are presented in ways that will make them most

broadly useful, especially in the indefinite future when current

methodologies or questions may come to be seen as

inadequate or parochial. Most critically, of course, the data

themselves must be permanently archived and available (e.g.,

sequence banks). I would urge, also, that a published phylogenetic

study include the results of as many broadly used

analytical procedures as possible, including those with which

the author strenuously disagrees. One loses nothing by presenting

both total-evidence trees and separate trees from, say,

morphological and molecular data sets, or trees with both

bootstrap and Bremer support values, or indeed, the results

of parsimony, maximum likelihood, and other analyses. By

all means, an author should assert preference for one or another

result, but the interests of scientific understanding—

both of the phylogeny of the clade and a broad range of

possible evolutionary or ecological questions—will best be

served if the “users” of the phylogeny can assess what the

range of alternatives might be. (And it is as poor a use of time

for the ecologist to rerun alternative analyses from the data

bank as for the systematist to revisit remote regions from

which the ecologist might have provided a synoptic tissue

collection!)

Second, many of the uses to which phylogenies may be

put profit from or even require large phylogenies that are as

complete as possible. Most published phylogenies are incomplete,

for understandable reasons of logistics or convenience.

However, inferences about temporal changes in speciation

and extinction rates, for example, might be made from phylogenies,

but only if all extant taxa are included (Barraclough

and Nee 2001). Moreover, tests of many hypotheses, using

36 The Importance of Knowing the Tree of Life

published phylogenies, are severely limited by the number

and reliability of phylogenies suitable to the particular problem

at hand; authors frequently use as examples only a few

phylogenies, which in some cases are quite controversial.

Because many questions in ecology and evolutionary biology

are questions of relative frequencies (e.g., the incidence

of various modes of speciation), phylogenies of many groups

will be needed. Thus, comprehensive phylogenies of large,

inclusive clades, such as the ever-growing tree of seed plants,

will be useful for many purposes we do not yet envision,

especially as these phylogenies become more complete. Although

the goal of a complete Tree of Life might not be attainable,

the journey toward it will enable us to address ever

more hypotheses ever more comprehensively.

Literature Cited

Avise, J. C. 1989. Gene trees and organismal histories: a

phylogenetic approach to population biology. Evolution

43:1192–1208.

Avise, J. C. 2000. Phylogeography: the history and formation of

species. Harvard University Press, Cambridge, MA.

Avise, J. C., and R. M. Ball, Jr. 1990. Principles of genealogical

concordance in species concepts and biological taxonomy.

Oxford Surv. Evol. Biol. 7:45–67.

Avise, J. C., and D. Walker. 1998. Pleistocene phylogeographic

effects on avian populations and the speciation process.

Proc. R. Soc. Lond. B 265:457–463.

Ballard, H. E., Jr., and K. J. Sytsma. 2000. Evolution and

biogeography of the woody Hawaiian violets (Viola,

Violaceae): arctic origins, herbaceous ancestry and bird

dispersal. Evolution 54:1521–1532.

Barraclough, T. G., P. Harvey, and S. Nee. 1995. Sexual

selection and taxonomic diversity in passerine birds. Proc.

R. Soc. Lond. B 259:211–215.

Barraclough, T. G., and S. Nee. 2001. Phylogenetics and

speciation. Trends Ecol. Evol. 16:391–399.

Barraclough, T. G., and A. P. Vogler. 2000. Detecting the

geographical pattern of speciation from species-level

phylogenies. Am. Nat. 155:419–434.

Basolo, A. L. 1996. The phylogenetic distribution of a female

preference. Syst. Biol. 45:290–307.

Baum, D. A., and K. L. Shaw. 1995. Genealogical perspectives

on the species problem. Pp. 289–303 in Experimental and

molecular approaches to plant biosystematics (P. C. Hoch

and A. G. Stephenson, eds.). Monographs in Systematic

Botany. Missouri Botanical Garden, St. Louis.

Berlocher, S. H. 1998. Can sympatric speciation via host or

habitat shift be proven from phylogenetic and biogeographic

evidence? Pp. 99–113 in Endless forms: species and

speciation (D. J. Howard and S. H. Berlocher, eds.). Oxford

University Press, New York.

Bermingham, E., and J. C. Avise. 1986. Molecular zoogeography

of freshwater fishes in the southeastern United States.

Genetics 113:939–965.

Bowler, P. J. 1983. The eclipse of Darwinism: anti-Darwinian

evolution theories in the decades around 1900. Johns

Hopkins University Press, Baltimore.

Bowler, P. J. 1996. Life’s splendid drama: evolutionary biology

and the reconstruction of life’s ancestry 1860–1940.

University of Chicago Press, Chicago.

Brooks, D. R., and D. R. Glen. 1982. Primates and pinworms: a

case study in coevolution. Proc. Helm. Soc. Wash. 49:76–85.

Brooks, D. R., and D. A. McLennan. 1991. Phylogeny, ecology,

and behavior. University of Chicago Press, Chicago.

Brown, W. L., Jr. 1959. General adaptation and evolution. Syst.

Zool. 7:157–168.

Brown, W. L., Jr., and E. O. Wilson. 1956. Character displacement.

Syst. Zool. 5:49–64.

Carroll, S. B., J. K. Grenier, and S. D. Weatherbee. 2001. From

DNA to diversity: molecular genetics and the evolution of

animal design. Blackwell Science, Malden, MA.

Chown, S. L., and K. J. Gaston. 2000. Areas, cradles and

museums: the latitudinal gradient in species richness.

Trends Ecol. Evol. 15:311–315.

Connell, J. H. 1971. On the role of natural enemies in preventing

competitive exclusion in some marine animals and in

rain forest trees. Pp. 298–310 in Dynamics of populations

(P. J. den Boer and G. R. Gradwell, eds.). Proceedings of the

Advanced Study Institute in Dynamics of Numbers in

Populations, Oosterbeck. Centre for Agricultural Publishing

and Documentation, Wageningen, the Netherlands.

Coyne, J. A., and H. A. Orr. 1989. Patterns of speciation in

Drosophila. Evolution 43:362–381.

Coyne, J. A., and T. D. Price. 2000. Little evidence for sympatric

speciation in island birds. Evolution 54:2166–2171.

Crandall, K. A., and A. R. Templeton. 1996. Applications of

intraspecific phylogenies. Pp. 81–99 in New uses for new

phylogenies (P. H. Harvey, A. J. Leigh Brown, J. Maynard

Smith, and S. Nee, eds.). Oxford University Press, Oxford.

Davis, M. B. 1976. Pleistocene biogeography of temperate

deciduous forests. Geosci. Man 13:13–26.

Dobzhansky, T., F. J. Ayala, G. L. Stebbins, and J. W. Valentine.

1977. Evolution. W. H. Freeman, San Francisco.

Dodson, E. O. 1960. Evolution: process and product. Reinhold,

New York.

Donoghue, M. J. 1989. Phylogenies and the analysis of evolutionary

sequences, with examples from seed plants.

Evolution 43:1137–1156.

Dowling, T. E., and C. L. Secor. 1997. The role of hybridization

and introgression in the diversification of animals. Annu.

Rev. Ecol. Syst. 28:593–619.

Eaton, T. H. 1970. Evolution. W. W. Norton, New York.

Edwards, A. W. F., and L. L. Cavalli-Sforza. 1964. Reconstruction

of evolutionary trees. Pp. 67–76 in Phenetic and

phylogenetic classification (V. H. Heywood and J. McNeill,

eds.). Publ. no. 6. Systematics Association, London.

Ehrlich, P. R., and R. W. Holm. 1963. The process of evolution.

McGraw-Hill, New York.

Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and plants: a

study in coevolution. Evolution 18:586–608.

Farrell, B. D. 1998. “Inordinate fondness” explained: why are

there so many beetles? Science 281:555–559.

Farrell, B. D., D. E. Dussourd, and C. Mitter. 1991. Escalation of

plant defense: do latex and resin canals spur plant diversification?

Am. Nat. 138:881–900.

Farrell, B. D., and C. Mitter. 1993. Phylogenetic determinants of

insect/plant community diversity. Pp. 253–266 in Species

The Fruit of the Tree of Life 37

diversity in ecological communities: historical and geographical

perspectives (R. E. Ricklefs and D. Schluter, eds.).

University of Chicago Press, Chicago.

Felsenstein, J. 1973. Maximum likelihood and minimum-steps

methods for estimating evolutionary trees from data on

discrete characters. Syst. Zool. 22:240–249.

Felsenstein, J. 1985. Phylogenies and the comparative method.

Am. Nat. 125:1–15.

Fitch, W. M. 1996. Uses for evolutionary trees. Pp. 116–133 in

New uses for new phylogenies (P. H. Harvey, A. J. Leigh

Brown, J. Maynard Smith, and S. Nee, eds.). Oxford

University Press, Oxford.

Funk, D. J., D. J. Futyma, G. Ortн, and A. Meyer. 1995. A

history of host associations and evolutionary diversification

for Ophraella (Coleoptera: Chrysomelidae): new evidence

from mitochondrial DNA. Evolution 491008–1017.

Futuyma, D. J. 1979. Evolutionary biology. 1st ed. Sinauer,

Sunderland, MA.

Futuyma, D. J. 1988. Sturm und Drang and the evolutionary

synthesis. Evolution 42:217–226.

Futuyma, D. J. 2000. Potential evolution of host range in

herbivorous insects. Pp. 42–53 in Host-specificity testing of

exotic arthropod biological control agents (R. Van Driesche,

T. Heard, A. McClay, and R. Reardon, eds.). U.S. Department

of Agriculture Forest Service, Morgantown, WV.

Futuyma, D. J., M. C. Keese, and D. J. Funk. 1995. Genetic

constraints on macroevolution: the evolution of host

affiliation in the leaf beetle genus Ophraella. Evolution

49:797–809.

Futuyma, D. J., M. C. Keese, and S. J. Scheffer. 1993. Genetic

constraints and the phylogeny of insect-plant associations:

responses of Ophraella communa (Coleoptera:

Chrysomelidae) to host plants of its congeners. Evolution

47:888–905.

Futuyma, D. J., and C. Mitter. 1996. Insect-plant interactions:

the evolution of component communities. Philos. Trans. R.

Soc. Lond. B 351:1361–1366.

Futuyma, D. J., and G. Moreno. 1988. The evolution of ecological

specialization. Annu. Rev. Ecol. Syst. 19:207–223.

Gittleman, J. L., C. G. Anderson, M. Kot, and H.-K. Luh. 1996.

Comparative tests of evolutionary lability and rates using

molecular phylogenies. Pp. 289–307 in New uses for new

phylogenies (P. H. Harvey, A. J. Leigh Brown, J. Maynard

Smith, and S. Nee, eds.). Oxford University Press, Oxford.

Givnish, T. J., and K. J. Sytsma (eds.). 1997. Molecular

evolution and adaptive radiation. Cambridge University

Press, New York.

Goodman, M., M. L. Weiss, and J. Czelusniak. 1982. Molecular

evolution above the species level: branching patterns, rates,

and mechanisms. Syst. Zool. 31:376–399.

Grant, V. 1977. Organismic evolution. W. H. Freeman, San

Francisco.

Guttman, D. S., and D. E. Dykhuizen. 1994. Clonal divergence

in Escherichia coli as a result of recombination, not mutation.

Science 266:1380–1383.

Hammer, M. F. 1995. A recent common ancestry for human Y

chromosomes. Nature 378:376–378.

Hare, M. P., F. Cipriano, and S. R. Palumbi. 2002. Genetic

evidence on the demography of speciation in allopatric

dolphin species. Evolution 56:804–816.

Harvey, P. H., and M. D. Pagel. 1991. The comparative method

in evolutionary biology. Oxford University Press, Oxford.

Hennig, W. 1950. Grundzьge einer Phylogenetischen Theorie

der Systematik. Deutscher Zentralverlag, Berlin.

Hillis, D. M. 2001. The emergence of systematic biology. Syst.

Biol. 50:301–303.

Holmes, E. C., P. L. Bollyky, S. Nee, A. Rambaut, G. P. Garnett,

and P. H. Harvey. 1996. Using phylogenetic trees to

reconstruct the history of infectious disease epidemics.

Pp. 169–186 in New uses for new phylogenies (P. H.

Harvey, A. J. Leigh Brown, J. Maynard Smith, and S. Nee,

eds.). Oxford University Press, Oxford.

Hubbell, S. P. 2001. The unified neutral theory of biodiversity

and biogeography. Princeton University Press, Princeton,

NJ.

Hudson, R. R. 1990. Gene genealogies and the coalescent

process. Oxford Surv. Evol. Biol. 7:1–44.

Hughes, A. L. 1999. Adaptive evolution of genes and genomes.

Oxford University Press, Oxford.

Hull, D. L. 1988. Science as a process: an evolutionary account

of the social and conceptual development of science.

University of Chicago Press, Chicago.

Humphries, C. J., and L. R. Parenti. 1999. Cladistic biogeography.

Oxford University Press, Oxford.

Ingman, M., H. Kaessmann, S. Pддbo, and U. Gyllensten. 2000.

Mitochondrial genome variation and the origin of modern

humans. Nature 408:708–713.

International Human Genome Sequencing Consortium. 2001.

Initial sequencing and analysis of the human genome.

Nature 409:860–921.

Janzen, D. H. 1970. Herbivores and the number of tree species

in tropical forests. Am. Nat. 104:501–528.

Kelley, S. T., and B. D. Farrell. 1998. Is specialization a dead

end? The phylogeny of host use in Dendroctonus bark

beetles (Scolytidae). Evolution 52:1731–1743.

Kimura, M. 1983. The neutral theory of molecular evolution.

Cambridge University Press, Cambridge.

Klicka, J., and R. M. Zink. 1997. The importance of recent ice

ages in speciation: a failed paradigm. Science 277:1666–

1669.

Kliman, R. M., P. Andolfatto, J. A. Coyne, F. Depaulis, M.

Kreitman, A. J. Berry, J. McCarter, J. Wakeley, and J. Hey.

2000. The population genetics of the origin and divergence

of the Drosophila simulans complex species. Genetics

156:1913–1931.

Kluge, A. G., and J. S. Farris. 1969. Quantitative phyletics and

the evolution of anurans. Syst. Zool. 18:1–32.

Knowles, L. L. 2000. Tests of Pleistocene speciation in montane

grasshoppers (genus Melanoplus) from the sky islands of

western North America. Evolution 54:1337–1348.

Knowles, L. L., D. J. Futuyma, W. F. Eanes, and B. Rannala.

1999. Insight into speciation from historical demography in

the phytophagous beetle genus Ophraella. Evolution

53:1846–1856.

Latham, R. E., and R. E. Ricklefs. 1993. Continental comparisons

of temperate-zone tree species diversity. Pp. 294–314

in Species diversity in ecological communities (R. E. Ricklefs

and D. Schluter, eds.). University of Chicago Press, Chicago.

Lee, M. Y. S., and R. Shine. 1998. Reptilian viviparity and

Dollo’s law. Evolution 52:1441–1450.

38 The Importance of Knowing the Tree of Life

Li, W.-H. 1997. Molecular evolution. Sinauer, Sunderland, MA.

Losos, J. B. 1992. The evolution of convergent structure in

Caribbean Anolis communities. Syst. Biol. 41:403–420.

Losos, J. B., T. R. Jackman, A. Larson, K. de Queiroz, and L.

Rodrнguez-Schettino. 1998. Contingency and determinism

in replicated adaptive radiations of island lizards. Science

279:2115–2118.

Louda, S. M., D. Kendall, J. Connor, and D. Simberloff. 1997.

Ecological effects of an insect introduced for biological

control of weeds. Science 277:1088–1090.

Lynch, M. 1990. The rate of morphological evolution from the

standpoint of the neutral expectation. Am. Nat. 136:727–

741.

Lynch, M., J. Blanchard, D. Houle, T. Kibota, S. Schultz, L.

Vassilieva, and J. Willis. 1999. Perspective: spontaneous

deleterious mutation. Evolution 53:645–663.

Martins, E. P. (ed.) 1996. Phylogenies and the comparative

method in animal behavior. Oxford University Press,

Oxford.

Maynard Smith, J., R. Burian, S. Kauffman, P. Alberch, J.

Campbell, B. Goodwin, R. Lande, D. Raup, and L. Wolpert.

1985. Developmental constraints and evolution. Quart. Rev.

Biol. 60:265–287.

Mayr, E. 1960. The emergence of evolutionary novelties.

Pp. 349–380 in The evolution of life (S. Tax, ed.). University

of Chicago Press, Chicago.

McCune, A. R., and N. J. Lovejoy. 1998. The relative rate of

sympatric and allopatric speciation in fishes: tests using

DNA sequence divergence between sister species and

among clades. Pp. 172–185 in Endless forms: species and

speciation (D. J. Howard and S. H. Berlocher, eds.). Oxford

University Press, New York.

McPeek, M. A. 1995. Morphological evolution mediated by

behavior in the damselflies of two communities. Evolution

49:749–769.

Milб, B., D. J. Girman, M. Kimura, and T. B. Smith. 2000.

Genetic evidence for the effect of a postglacial population

expansion on the phylogeography of a North American

songbird. Proc. R. Soc. Lond. B 267:1033–1040.

Mitter, C., and D. R. Brooks. 1983. Phylogenetic aspects of

coevolution. Pp. 65–98 in Coevolution (D. J. Futuyma and

M. Slatkin, eds.). Sinauer, Sunderland, Mass.

Mitter, C., B. Farrell, and B. Wiegmann. 1988. The phylogenetic

study of adaptive zones: has phytophagy promoted insect

diversification? Am. Nat. 132:107–128.

Mooers, A. Ш., and S. B. Heard. 1997. Inferring evolutionary

process from phylogenetic tree shape. Q. Rev. Biol. 72:31–

54.

Moritz, C. 1994. Defining evolutionary significant units for

conservation. Trends Ecol. Evol. 9:373–375.

Morrone, J. J., and J. V. Crisci. 1995. Historical biogeography:

introduction to methods. Annu. Rev. Ecol. Syst. 26:373–

401.

Nelson, G., and N. I. Platnick. 1981. Systematics and biogeography:

cladistics and vicariance. Columbia University Press,

New York.

Nosil, P. 2002. Transition rates between specialization and

generalization in phytophagus insects. Evolution 56:1701–

1706.

Page, R. D. M., and M. S. Hafner. 1996. Molecular phylogenies

and host-parasite cospeciation: gophers and lice as a model

system. Pp. 255–270 in New uses for new phylogenies

(P. H. Harvey, A. J. Leigh Brown, J. Maynard Smith, and

S. Nee, eds.). Oxford University Press, Oxford.

Purvis, A., P.-M. Agapow, J. L. Gittleman, and G. M. Mace.

2000a. Non-random extinction and the loss of evolutionary

history. Science 288:328–330.

Purvis, A., J. L. Gittleman, G. Cowlishaw, and G. M. Mace.

2000b. Predicting extinction risk in declining species. Proc.

R. Soc. Lond. B 267:1947–1952.

Qian, H., and R. E. Ricklefs. 1999. A comparison of the

taxonomic richness of vascular plants in China and the

United States. Am. Nat. 154:160–181.

Raxworthy, C. J., M. R. J. Forstner, and R. A. Nussbaum. 2002.

Chameleon radiation by oceanic dispersal. Nature 415:784–

787.

Richardson, J. E., R. T. Pennington, T. D. Pennington, and P. M.

Hollingsworth. 2001. Rapid diversification of a species-rich

genus of neotropical rain forest trees. Science 293:2242–

2245.

Rieseberg, L. H. 1997. Hybrid origins of plant species. Annu.

Rev. Ecol. Syst. 28:359–389.

Ryan, M. J., and A. S. Rand. 1993. Sexual selection and signal

evolution—the ghost of biases past. Philos. Trans. R. Soc.

Lond. B 340:187–195.

Sanderson, M. J., and M. J. Donoghue. 1996. Reconstructing

shifts in diversification rate on phylogenies. Trends Ecol.

Evol. 11:15–20.

Sanderson, M. J., and L. Hufford (eds.). 1996. Homology: the

recurrence of similarity in evolution. Academic Press, San

Diego.

Savage, J. M. 1963. Evolution. Holt, Rinehart and Winston,

New York.

Schliewen, U. K., D. Tautz, and S. Pддbo. 1994. Sympatric

speciation suggested by monophyly of crater lake cichlids.

Nature 368:629–632.

Schluter, D. 2000. The ecology of adaptive radiation. Oxford

University Press, Oxford.

Sidor, C. A., and J. A. Hopson. 1998. Ghost lineages and

“mammalness”: assessing the temporal pattern of character

acquisition in the Synapsida. Paleobiology 24:254–273.

Sillйn-Tullberg, B. 1988. Evolution of gregariousness in

aposematic butterfly larvae: a phylogenetic analysis.

Evolution 42:293–305.

Silvertown, J., M. Franco, and J. L. Harper (eds.). 1997. Plant

life histories: ecology, phylogeny and evolution. Cambridge

University Press, Cambridge.

Sokal, R. R., and C. D. Michener. 1958. A statistical method for

evaluating systematic relationships. Univ. Kansas Sci. Bull.

38:1409–1438.

Stebbins, G. L. 1966. Processes of organic evolution. Prentice-

Hall, Englewood Cliffs, NJ.

Stebbins, G. L. 1974. Flowering plants: evolution above the

species level. Harvard University Press, Cambridge, MA.

Taberlet, P., L. Fumagalli, A.-G. Wust-Saucy, and J.-F. Cosson,

1998. Comparative phylogeography and postglacial

colonization routes in Europe. Mol. Ecol. 7:453–464.

Takahata, N., Y. Satta, and J. Klein. 1995. Divergence time and

population size in the lineage leading to modern humans.

Theor. Popul. Biol. 48:198–221.

The Fruit of the Tree of Life 39

Throckmorton, L. H. 1965. Similarity versus relationship in

Drosophila. Syst. Zool. 14:221–236.

Vane-Wright, R. I., C. J. Humphries, and P. H. Williams. 1991.

What to protect—systematics and the agony of choice. Biol.

Conserv. 55:235–254.

Venter, J. C., M. D. Adams, E. W. Myers, P. W. Li, R. J. Mural,

G. G. Sutton, H. V. Smith, M. Yandell, C. A. Evans, et al.

2001. The sequence of the human genome. Science

291:1304–1351.

Volpe, E. P. 1970. Understanding evolution, 2nd ed. Wm. C.

Brown, Dubuque, IA.

Wagner, G. P. 1989. The biological homology concept. Annu.

Rev. Ecol. Syst. 20:51–69.

Wahlberg, N. 2001. The phylogenetics and biochemistry

of host-plant specialization in melitaeine butterflies

(Lepidoptera: Nymphalidae). Evolution 55:522–

537.

Wakeley, J., and J. Hey. 1997. Estimating ancestral population

parameters. Genetics 145:847–855.

Webb, C. O. 2000. Exploring the phylogenetic structure of

ecological communities: an example for rain forest trees.

Am. Nat. 156:145–155.

Westoby, M., M. R. Leishman, and J. M. Lord. 1995. On

misinterpreting the “phylogenetic correction.” J. Ecol.

83:531–534.

Wilson, A. C., S. S. Carlson, and T. J. White. 1977. Biochemical

evolution. Annu. Rev. Biochem. 46:573–639.

Zink, R. M., R. C. Blackwell-Rago, and F. Ronquist. 2000. The

shifting roles of dispersal and vicariance in biogeography.

Proc. R. Soc. Lond. B 267:497–503.

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