Jerry A. Coyne

Patterns of speciation in Drosophila

To investigate the time course of speciation, we gathered literature data on 119 pairs of closely related Drosophila species with known genetic distances, mating discrimination, strength of hybrid sterility and inviability, and geographic ranges. Because genetic distance is correlated with divergence time, these data provide a cross‐section of taxa at different stages of speciation.

Theory and speciation

The study of speciation has become one of the most active areas of evolutionary biology, and substantial progress has been made in documenting and understanding phenomena ranging from sympatric speciation and reinforcement to the evolutionary genetics of postzygotic isolation. This progress has been driven largely by empirical results, and most useful theoretical work has concentrated on making sense of empirical patterns. Given the complexity of speciation, mathematical theory is subordinate to verbal theory and generalizations about data. Nevertheless, mathematical theory can provide a useful classification of verbal theories; can help determine the biological plausibility of verbal theories; can determine whether alternative mechanisms of speciation are consistent with empirical patterns; and can occasionally provide predictions that go beyond empirical generalizations. We discuss recent examples of progress in each of these areas.

THE LOCUS OF EVOLUTION: EVO DEVO AND THE GENETICS OF ADAPTATION

Abstract An important tenet of evolutionary developmental biology (“evo devo”) is that adaptive mutations affecting morphology are more likely to occur in the cis-regulatory regions than in the protein-coding regions of genes. This argument rests on two claims: (1) the modular nature of cis-regulatory elements largely frees them from deleterious pleiotropic effects, and (2) a growing body of empirical evidence appears to support the predominant role of gene regulatory change in adaptation, especially morphological adaptation. Here we discuss and critique these assertions. We first show that there is no theoretical or empirical basis for the evo devo contention that adaptations involving morphology evolve by genetic mechanisms different from those involving physiology and other traits. In addition, some forms of protein evolution can avoid the negative consequences of pleiotropy, most notably via gene duplication. In light of evo devo claims, we then examine the substantial data on the genetic basis of adaptation from both genome-wide surveys and single-locus studies. Genomic studies lend little support to the cis-regulatory theory: many of these have detected adaptation in protein-coding regions, including transcription factors, whereas few have examined regulatory regions. Turning to single-locus studies, we note that the most widely cited examples of adaptive cis-regulatory mutations focus on trait loss rather than gain, and none have yet pinpointed an evolved regulatory site. In contrast, there are many studies that have both identified structural mutations and functionally verified their contribution to adaptation and speciation. Neither the theoretical arguments nor the data from nature, then, support the claim for a predominance of cis-regulatory mutations in evolution. Although this claim may be true, it is at best premature. Adaptation and speciation probably proceed through a combination of cis-regulatory and structural mutations, with a substantial contribution of the latter.

PERSPECTIVE : A CRITIQUE OF SEWALL WRIGHT'S SHIFTING BALANCE THEORY OF EVOLUTION

We evaluate Sewall Wrights three‐phase “shifting balance” theory of evolution, examining both the theoretical issues and the relevant data from nature and the laboratory. We conclude that while phases I and II of Wrights theory (the movement of populations from one “adaptive peak” to another via drift and selection) can occur under some conditions, genetic drift is often unnecessary for movement between peaks. Phase III of the shifting balance, in which adaptations spread from particular populations to the entire species, faces two major theoretical obstacles: (1) unlike adaptations favored by simple directional selection, adaptations whose fixation requires some genetic drift are often prevented from spreading by barriers to gene flow; and (2) it is difficult to assemble complex adaptations whose constituent parts arise via peak shifts in different demes. Our review of the data from nature shows that although there is some evidence for individual phases of the shifting balance process, there are few empirical observations explained better by Wrights three‐phase mechanism than by simple mass selection. Similarly, artificial selection experiments fail to show that selection in subdivided populations produces greater response than does mass selection in large populations. The complexity of the shifting balance process and the difficulty of establishing that adaptive valleys have been crossed by genetic drift make it impossible to test Wrights claim that adaptations commonly originate by this process. In view of these problems, it seems unreasonable to consider the shifting balance process as an important explanation for the evolution of adaptations.

The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster

The cuticular hydrocarbon (CH) pheromones in Drosophila melanogaster exhibit strong geographic variation. African and Caribbean populations have a high ratio of 5,9 heptacosadiene/7,11 heptacosadiene (the “High” CH type), whereas populations from all other areas have a low ratio (“Low” CH type). Based on previous genetic mapping, DNA markers were developed that localized the genetic basis of this CH polymorphism to within a 13-kb region. We then carried out a hierarchical search for diagnostic nucleotide sites starting with four lines, and increasing to 24 and 43 lines from a worldwide collection. Within the 13-kb region, only one variable site shows a complete concordance with the CH phenotype. This is a 16-bp deletion in the 5′ region of a desaturase gene (desat2) that was recently suggested to be responsible for the CH polymorphism on the basis of its expression [Dallerac, R., Labeur, C., Jallon, J.-M., Knipple, D. C., Roelofs, W. L. & Wicker-Thomas, C. (2000) Proc. Natl. Acad. Sci. 97, 9449–9454]. The cosmopolitan Low type is derived from the ancestral High type, and DNA sequence variations suggest that the former spread worldwide with the aid of positive selection. Whether this CH variation could be a component of the sexual isolation between Zimbabwe and other cosmopolitan populations remains an interesting and unresolved question.

Sperm competition between Drosophila males involves both displacement and incapacitation

Females in almost all animal groups copulate with multiple males,. This behaviour allows different males to compete for fertilization and gives females the opportunity to mediate this competition. In many animals and most insects, the second male to copulate with a female typically sires most of her offspring,,. In Drosophila melanogaster, this second-male sperm precedence has long been studied but, as in most species, its mechanism has remained unknown. Here we show, using labelled sperm in doubly mated females, that males can both physically displace andincapacitate stored sperm from earlier-mating males. Displacement occurs only if the second male transfers sperm to the female, and in only one of her three sperm-storage organs. Incapacitation can be caused by either fertile or spermless second males, but requires extended intervals between matings. Sperm from different males are not ‘stratified’ in the storage organs but mix freely. Many animal species may have multiple mechanisms of sperm competition like those observed here, and revealing these mechanisms is necessary to understand the genetic and evolutionary basis of second-male sperm precedence in animals.

Bergmann’s rule in ectotherms: is it adaptive?

. 1986. Predicting body size with life history models. Bioscience 36:316-323. SCOTT, S. M., AND H. DINGLE. 1990. Developmental programmes and adaptive syndromes in insect life-cycles. Pp. 69-85 in F Gilbert, ed. Insect life cycles: Genetics, evolution and co-ordination. Springer-Verlag, London. VAN VOORHIES, W. A. 1996. Bergmann size clines: A simple explanation for their occurrence in ectotherms. Evolution 50:12591264.

LITTLE EVIDENCE FOR SYMPATRIC SPECIATION IN ISLAND BIRDS

It has been suggested that the presence of sister species in small circumscribed areas, such as isolated lakes or islands, might imply that these species originated sympatrically. To investigate this possibility in birds, we searched for endemic, congeneric species on isolated islands in the ocean. Among 46 islands and small archipelagos chosen because they contain at least one species of endemic land bird, we identified seven pairs of endemic congeners (excluding flightless rails). Of these seven, only four pairs are potentially sister species and thus possible candidates for sympatric speciation. However, three of these four pairs have always been considered the results of double invasion from a mainland source (in two of these cases, molecular‐phylogenetic work has either confirmed a double invasion or is ambiguous). The one remaining pair may have speciated allopatrically on a small archipelago. Additional phylogenetic studies are required to understand these cases, and our results should also be considered in light of the large number of island‐bird extinctions in historic time. We conclude that, at present, there is little evidence for sympatric speciation in island birds.

A Test of the Snowball Theory for the Rate of Evolution of Hybrid Incompatibilities

Rolling Snowballs The genetic incompatibilities that separate ongoing speciation events have been hypothesized by the Dobzhansky-Muller model of speciation to snowball—that is, accumulate mutations causing postzygotic isolation at a faster rate than the linear accumulation of mutations. This occurs because of potential deleterious epistatic interactions in hybrids involving two or more interacting genes. Testing QTLs (quantitative trait loci) in seed and pollen sterility between multiple species pairs in the plant group Solanum, Moyle and Nakazato (p. 1521) show that hybrid female (seed) sterility accumulates exponentially between increasingly distant species pairs, although not for hybrid male (pollen) sterility. In contrast, loci contributing to differences in other traits show no evidence for nonlinear accumulation over time. Matute et al. (p. 1518) come to similar conclusions through the use of deletion mapping in comparisons between two pairs of species of Drosophila. The number of genes causing postzygotic isolation grows as fast as the square of the number of substitutions between two species. Thus, a hybrid snowball effect is found in both plants and animals. Two studies support the theory that the number of genes involved in hybrid incompatibility increases faster than linearly. Hybrids between species are often sterile or inviable because the long-diverged genomes of their parents cause developmental problems when they come together in a single individual. According to the Dobzhansky-Muller (DM) model, the number of genes involved in these “intrinsic postzygotic incompatibilities” should increase faster than linearly with the divergence time between species. This straightforward prediction of the DM model has remained contentious owing to a lack of explicit tests. Examining two pairs of Drosophila species, we show that the number of genes involved in postzygotic isolation increases at least as fast as the square of the number of substitutions (an index of divergence time) between species. This observation verifies a key prediction of the DM model.

CRYPTIC REPRODUCTIVE ISOLATION IN THE DROSOPHILA SIMULANS SPECIES COMPLEX

Forms of reproductive isolation that act after copulation but before fertilization are potentially important components of speciation, but are studied only infrequently. We examined postmating, prezygotic reproductive isolation in three hybridizations within the Drosophila simulans species complex. We allowed females to mate only once, observed and timed all copulations, dissected a subset of the females to track the storage and retention of sperm, examined the number and hatchability of eggs laid after insemination, counted all progeny produced, and measured the longevity of mated females. Each of the three hybridizations is characterized by a different set of cryptic barriers to heterospecific fertilization. When D. simulans females mate with D. sechellia males, few heterospecific sperm are transferred, even during long copulations. In contrast, copulations of D. simulans females with D. mauritiana males are often too short to allow sperm transfer. Those that are long enough to allow insemination, however, involve the transfer of many sperm, but only a fraction of these heterospecific sperm are stored by females, who also lay fewer eggs than do D. simulans females mated with conspecific males. Finally, when D. mauritiana females mate with D. simulans males, sperm are transferred and stored in abundance, but are lost rapidly from the reproductive tract and are therefore used inefficiently. These results add considerably to the list of reproductive isolating mechanisms in this well‐studied clade and possibly to the list of evolutionary processes that could contribute to their reproductive isolation.