books and arts A duet on speciation A synthesis of ideas about how species arise hits the right note. Speciation species are? Having grown by Jerry A. Coyne & H. Allen Orr impatient over what they Sinauer: 2004. 545 pp. $89.95 (hbk); $54.95, feel are pointless philo- £35.99 (pbk) sophical or (worse) seman- Axel Meyer tic debates over the species BETTMANN/CORBIS problem, Coyne and Orr Identifying and understanding the processes advocate the collection of that lead to the origin of species is one more data on speciation of the fundamental problems of evolution. and fewer debates on what Solving it requires not only field studies, species are. They conclude comparative analyses and lab work, but also that it doesn’t really matter a scholarly knowledge of previous work. to which particular species Speciation,a joyous duet by two of the concept one subscribes. field’s leading soloists, Jerry Coyne and I have painted a picture Allen Orr, should help. This treasure trove that is bleaker than it really of knowledge, which provides ample food is. Most biologists since for thought, succinctly outlines hypotheses Darwin have believed that and proposes research programmes to species are real. The biolo- test them. gical species concept (BSC) The literature on speciation spans more proposed by Mayr and than a century and a half, and includes con- Theodosius Dobzhansky is tributions from experimenters, innovative the most prominent and thinkers and theoreticians. A vast jungle of widely accepted one. It empirical data has accumulated, but every defines species as “groups single tree must still be inspected carefully of actually or potentially to develop a comprehensive picture of the interbreeding natural pop- entire forest. The empirical evidence must ulations, which are repro- then be analysed rigorously to see how it ductively isolated from fits with alternative models, to distinguish Going separate ways: divergence and speciation in the herring family. other such groups”. Thus, between competing hypotheses. Coyne and new species arise when Orr have succeeded in this task. speciation? Darwin largely ignored this issue reproductive isolation separates formerly But why, almost 150 years after the publi- as well and,at least in On the Origin of Species, interbreeding populations. cation of Darwin’s On the Origin of Species, seemed to treat species as if they are not Like most researchers,Coyne and Orr feel is there still so much left to say and do? Sur- even real in the philosophical sense. To that the study of speciation is helped,or even prisingly, Darwin did not directly address him, species were convenient constructs — only becomes possible, by accepting the the question of the origin of species in his groupings of sets of individuals that resem- BSC and focusing on the study of reproduc- published writings. For him, the origin of ble each other, but which are not distinct, tive isolation. They want to know where, adaptations to new ecological challenges being just artificially united fluctuating how and when reproductive isolation comes within species and the origin of the species forms that overlap with other potential about, and how it can be measured. How- themselves seemed almost the same thing. species. To overstate the dilemma, Darwin ever, some researchers believe that accept- Arguably, the processes that result in the neither believed in species nor did he write ing the BSC stifles the study of speciation divergence of lineages to form new species are about how new species arise. He left these by limiting it to the study of the origin of different from the mechanisms of the longer, really hard nuts for subsequent generations reproductive isolation.The concept’s depen- and often more pronounced, divergence of evolutionary biologists to crack. dence on reproductive isolation among sex- that occurs afterwards. It is generally accep- Ernst Mayr, the centenarian doyen of ually reproducing organisms, for example, ted that the processes differ in timescale: evolutionary biology, contends that the means it cannot easily be applied to bacteria whether species arise rapidly (for example species problem can be reduced to a simple and organisms that reproduce clonally. through polyploidation, as in some plants) choice between species as realities of nature Geographic mechanisms of speciation,in or more gradually, the splitting of lineages or as theoretical constructs of the human which formerly interbreeding populations is generally much faster than the subsequent mind.There are many alternative definitions are prevented from doing so by geographic divergence within a species. But are the of species, each emphasizing some cause or barriers,are generally thought to be the most processes through which divergence occurs biological feature of species, and/or basing common way for new species to arise, and during and after speciation fundamentally its definition on a particular analytical or this idea receives much empirical support. different? Coyne and Orr would probably empirical approach or data set in an attempt A non-adaptive by-product of isolation is say yes;others might disagree. to capture the essence of what makes a group that, over many generations, genomes or The study of speciation depends on the of individuals a species. (Thankfully, these gene frequencies drift apart. This then pre- ‘species problem’ — knowing what consti- are discussed in the appendix of the book.) vents interbreeding and the homogenizing tutes a species. How objective are the criteria Some researchers have even advocated abol- flow of genes from one species to the other that we use to assign individuals and pop- ishing the notion of species altogether. when they come into contact again. ulations to units that we call species, and Can we even begin to answer questions It was Mayr who laid the foundations for do they affect the study of the processes of about speciation without knowing what much of the current research on the origin NATURE | VOL 431 | 23 SEPTEMBER 2004 | www.nature.com/nature 399 © 2004 Nature Publishing Group books and arts of species, in particular for the BSC and for most geography-based hypotheses of specia- tion. Coyne and Orr could be accused of being ‘admayrers’, but that’s not the worst thing one can be called, in my opinion. Unlike Mayr in his early work, the authors M. PETERSON/CORBIS admit, albeit with palpable hesitation, that speciation can also occur without geographic isolation,in overlapping or ‘sympatric’areas. Sympatric speciation,which for decades had all the caché of a four-letter word, is increas- ingly seen to be responsible for the origin of at least a minority of species. Coyne and Orr also give renewed cre- dence to models of speciation that empha- size a role for sexual or natural selection, rather than viewing the origin of species as little more than a by-product of isolation. One currently popular model, ecological speciation, de-emphasizes geographical set- Grabbing a bite: the main role of teeth is to break down large items of food into smaller ones. tings and reaffirms the importance of local adaptations and natural selection in bring- influence this.He also includes more general ing about speciation.Reproductive isolation reviews of dental and oral anatomy,and pro- may be brought about by ecological pro- Something to vides an excellent summary of the processes cesses, such as habitat fragmentation or the of chewing and oral transport, viewed from uneven distribution of resources. In such chew on the perspective of the mechanical properties cases, interbreeding is prevented between Dental Functional Morphology: of food,such as particle size and stickiness. populations that are limited — by behav- How Teeth Work This food’s-eye view leads to numerous ioural, physiological and morphological by Peter W. Lucas insights and interesting ideas,such as Lucas’s adaptations — to a very particular set of Cambridge University Press: 2004. 372 pp. theory of fracture scaling. Bigger animals prey items, for example, or a particular tree $130, £75 have bigger teeth, whose surface areas might species that they need to build their nests. Daniel E. Lieberman be predicted to scale with body mass to the The absence of the homogenizing effect of power of 0.67 (because tooth area increases gene flow between individuals, not through Science has made substantial progress since to the power of two,and body mass increases geography but by the divergence of Aristotle wrote (apparently without doing to the power of three, yielding a scaling ratio adapted and ecologically important traits, much research) that women have fewer of 2/3). Yet tooth surface area in mammals possibly even in the same environment, then teeth than men. The sheer volume of pub- typically scales to the power of 0.61.Why this leads to reproductive isolation. In this way, lished research on teeth since may lead some is so remains elusive, but Lucas argues that natural selection can play a prominent role to conclude that we have over-compensated fracture mechanics plays a role. in speciation. for Aristotle’s ignorance. Yet teeth merit all The argument is complex,but boils down The most recent work, largely done on this attention because of their tremendous to the observation that once a crack is initiated fish models, includes modern genomic biological importance — not to mention the in an object,little additional energy is needed approaches, such as the analysis of quantita- dreadful pain they can cause. Dental devel- to finish the job, regardless of its size. Bigger tive trait loci. It concludes that reproductive opment and function are the focus of much foods fracture at relatively low stress, which isolation and speciation may be a by-product clinical attention. And for evolutionary biol- has several implications. One is that bigger of ecological differences and disruptive ogists, teeth are invaluable sources of infor- animals (assuming that they chew bigger selection on a surprisingly small number of mation about taxonomy, phylogeny and food) need relatively less muscle force (as phenotypic traits,which are controlled by an many other aspects of animal biology.