When houseguests become parasites: Sympatric speciation in ants Stewart H. Berlocher* Department of Entomology, University of Illinois at Urbana–Champaign, 320 Morrill Hall, 505 South Goodwin Avenue, Urbana, IL 61801 pecies are part of the common related species, and we are finally, if still argue that sympatric speciation was not coinage of biology. Taxonomists dimly, seeing some of the specific genes limited to a handful of special cases, but name them, developmental biolo- that underlie reproductive isolation (3). was quite common. Bush was driven to gists deconstruct them, physiolo- But fundamental questions remain his stance by the observation that one S unanswered. A critical question is how gists compare them, ecologists count could find many groups of closely re- them, conservation biologists conserve reproductive isolation could evolve in lated, sympatric species that use differ- them, and evolutionary biologists study the face of gene flow; random mating ent ecological niches. Conspicuous their multiplication and extinction. It within a population and gene flow be- among these groups are parasites of ani- may be that only the individual is a tween neighboring populations are enor- mals and plants, which are often highly more important biological unit than the mously powerful homogenizing forces. specialized ecologically and frequently species. It is thus no surprise that Dar- How could selection tear a single popu- mate on the host, a factor that poten- win named his great work On the Origin lation into two reproductively isolated tially links any adaptation to a new host of Species, nor is it a surprise that many with a reduction in gene flow between evolutionary biologists today concen- the new and ancestral populations. trate their efforts on understanding spe- We might expect Another group of organisms that has cies formation, or speciation. Riitta attracted undying speculation about Savolainen and Kari Vepsa¨la¨inen (1), in to see speciation in sympatric speciation are the social para- a study in this issue of PNAS, have con- sites in the Hymenoptera (7). Social tributed significantly to a long-standing response to humanity’s parasites of the wasps, ants, and bees debate in evolutionary biology, over have fascinating natural histories. Of the whether geographic isolation is a neces- modification of usual social insect divisions into female sary first step in speciation, in a study of reproductives (queens), males, and non- social parasites in Myrmica ants (2). The the globe. reproductive females (workers), only resolution of this argument has impor- two occur in social parasites: female re- tant consequences beyond evolutionary productive and males (7). Workers are biology. If species do not have to wait species? For Darwin, who had an over- often totally absent. Social parasite spe- for the next geological event to speciate, riding faith in the power of natural se- cies live by tricking workers of the host then speciation could conceivably be lection, this was not a difficulty. But species into feeding themselves and their very rapid. This, in turn, means that the with the mathematical sophistication progeny. They are the ultimate bad process might be conducive to study in that the new science of population ge- houseguests. Social parasites occur in real time. We might expect to see spe- netics brought to the ‘‘modern synthe- most groups of social Hymenoptera, in- ciation in response to humanity’s inces- sis’’ of the 1930s (4) came an under- cluding bumble bees, several wasp sant modification of the globe. Anthro- standing of just how strong selection groups, and many ant groups. pogenic change might drive not only had to be to overcome gene flow. The How does social parasitism involve such well known adaptations as the evo- solution that Ernst Mayr, Theodosius sympatric speciation? The entomologist lution of insecticide, herbicide, and anti- Dobzhansky, and others (5) proposed is Emery in 1909 noted that social para- biotic resistance, but also, for example, that geographic barriers could break the sites almost always parasitized close rel- speciation of herbivorous insects adapt- chain of gene flow between populations. atives, an observation now known as ing to plants moved to new parts of the If two populations exchange no genes ‘‘Emery’s rule’’ (7). Others in the de- world. because of geographic isolation, then cades since (7) have been entranced by To fully understand Savolainen and these populations can evolve completely the idea that the social parasites could Vepsa¨la¨inen’s results, some history is in independently, adapting to new chal- evolve from their hosts. The most often order. In the 144 years since publication lenges until genetic reproductive isola- proposed scenario is evolution from a of On the Origin of Species, enormous tion evolves as an evolutionary byprod- state of polygyny (multiple queens) progress has been made in illuminating uct. The two new species that have within a species that all share equally in the things we need to know to under- evolved in geographic isolation (or allo- worker production, to polygyny with stand speciation (2). We now know a lot patry) can later coexist in the same area some queens ‘‘cheating’’ to increase about geographic isolation and the bio- (in sympatry). Geographic (or allopat- their fitness by producing mostly repro- geography of closely related species. We ric) speciation is such an obvious solu- ductives, to assortative mating among know the kinds of features that prevent tion to the problem of evolving repro- cheaters, to finally a new parasitic spe- mating between closely related species ductive isolation, and the evidence for it cies reproductively isolated from its an- or, in other words, that produce ‘‘repro- so great (5), that it became the only ac- cestor (1, 7). Such a sympatric process ductive isolation.’’ We understand that cepted mode of speciation (excepting would produce species pairs that are many close species differ in ecology, and speciation via polyploidy and a few sister species (nearest relatives), which we appreciate the consequences of lack other similar mechanisms, which must of ecological differences. We know a occur in sympatry). great deal about how to count differ- But a few evolutionary biologists, such See companion article on page 7169. ences between the genomes of closely as Guy Bush (6), started in the 1960s to *E-mail: [email protected]. 6896–6898 ͉ PNAS ͉ June 10, 2003 ͉ vol. 100 ͉ no. 12 www.pnas.org͞cgi͞doi͞10.1073͞pnas.1332533100 Downloaded by guest on September 30, 2021 COMMENTARY should pair together in a phylogenetic tree. But in evolutionary biology it can be a long, rocky road from scenario to proof. ‘‘Proving’’ sympatric speciation has been a particularly tough proposi- tion. The only potentially simple cases involve divergence in historical time (8, 9). For example, the apple host race of the fruit fly Rhagoletis pomonella arose from the ancestral, native, hawthorn- infesting population in North America Ϸ140 years ago, and has evolved sub- stantial reproductive isolation from the ancestral race. The catch here, however, Fig. 1. (A) Species tree (blue area) and allele tree (lines). Sampling just one allele per species reveals only is that reproductive isolation between part of what could be known about a speciation (red allele branches, or clades), whereas sampling the races is only partial; they are not extensively (red ϩ light brown clades) reveals much more about timing, geographical patterns of events, generally accepted as “complete” etc. Dark brown extinct clades are unknowable. (B) Allele tree for a host (red) and parasite (green) that species. would support sympatric speciation, because the parasite is not only sister species to the host but also For the vast majority of cases, the hy- originated later than the host (parasite alleles originate at a later time). (C) A pattern that has been pothesis of sympatric speciation must observed for mitochondrial genes implying both interspecific gene flow and rapid evolution, possibly stand or fall based on inferences about because of ‘‘selective sweeps’’ of selected mutations through the species (tree labeled as in B). the evolutionary past. This is certainly true for hymenopteran social parasites; history of the Myrmica social parasites ever since the pioneering work of Avise it is unlikely that we will see the evolu- would facilitate preferential mating be- and colleagues (10) in the late 1970s, tion of new ones in historical time. What kinds of observations can be used tween newly originated parasites (1). very intricate and informative genealogi- to test the competing hypotheses of Using the powerful tools of modern cal relationships of haplotypes (or al- sympatric and allopatric speciation in phylogeny estimation based on molecu- leles) exist within species trees. Such a the past? Fundamentally, they are (i) lar data, it is now possible to infer phy- ‘‘gene tree’’ within a ‘‘species tree’’ is the types of intermediate stages seen logenies with some confidence. As shown in Fig. 1A. When only one allele and (ii) the phylogenetic relationships Savolainen and Vepsa¨la¨inen point out, a is sampled per species or population, as observed in the relevant populations relatively simple and straightforward is the case for most of Savolainen and and species. inference is that if the parasites and Vepsa¨la¨inen’s work, then one can see Over many decades, Ernst Mayr has hosts each form a monophyletic group, only allele clades like those shown in pointed out that a parasite could adapt then sympatric speciation can be cleanly red in Fig. 1. Such sampling is suitable to a new host in a geographically iso- rejected. That is, if one finds that the for determining relationships at the spe- lated population, evolve reproductive social parasites are all grouped together cies and higher level. However, other isolation there, and then come back into on one branch or clade of a phyloge- extant lineages, like those shown in light sympatry with the original form (5).