William R. Rice

Laboratory experiments on speciation : what have we learned in 40 years ?

We integrate experimental studies attempting to duplicate all or part of the speciation process under controlled laboratory conditions and ask what general conclusions can be made concerning the major models of speciation. Strong support is found for the evolution of reproductive isolation via pleiotropy and/or genetic hitchhiking with or without allopatry. Little or no support is found for the bottleneck and reinforcement models of speciation. We conclude that the role of geographical separation in generating allopatry (i.e., zero gene flow induced by spatial isolation) has been overemphasized in the past, whereas its role in generating diminished gene flow in combination with strong, discontinuous, and multifarious divergent selection, has been largely unappreciated.

PERSPECTIVE: CHASE-AWAY SEXUAL SELECTION: ANTAGONISTIC SEDUCTION VERSUS RESISTANCE

A model of sexual selection that leads to the evolution of exaggerated male display characters that is based on antagonistic coevolution between the sexes is described. The model is motivated by three lines of research: intersexual conflict with respect to mating, sensory exploitation, and the evolution of female resistance, as opposed to preference, for male display traits. The model generates unique predictions that permit its operation to be distinguished from other established models of sexual selection. One striking prediction is that females will frequently win the coevolutionary arms race with males, leaving them encumbered with costly ornaments that have little value except that their absence understimulates females. Examples from the literature suggest that the model may have broad application in nature. The chase‐away model is a special case of the more general phenomenon of Interlocus Contest Evolution (ICE).

Dangerous liaisons

Naturalists have long known that copulation can be dangerous to females. For example, female waterfowl sometimes drown while being mated by multiple males (1). Beyond this type of anecdotal information, detailed quantification of the cost of mating in wild populations of waterstrides has demonstrated that: (i) males attempt to copulate with females at a rate that far exceeds what is needed to fertilize her eggs, (ii) males increase their fitness by mating at this high rate, and (iii) female fitness is reduced by supernumerary copulations (2, 3).

The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen

Abstract Different loci within the genome of a single species can potentially coevolve in a manner that is analogous to the Red Queen process among species. The major factor driving this antagonistic coevolution among loci is intergenomic conflict, i.e., discord between individuals that is mediated by two or more gene products that are derived from different gene loci. We conclude that antagonistic coevolution is common among loci that code for social interactions, and that it has broad evolutionary implications, especially in the context of speciation and sex chromosome evolution.

Intersexual ontogenetic conflict

Evolutionary conflict has been investigated at many levels of organization, from interactions between loci within a genome to the coevolution of species. Here we review evidence for intersexual ontogenetic conflict, a type of conflict that has received relatively little attention both theoretically and empirically. It is manifest during development when expression of the same allele, on average, moves one sex towards, and the other sex away from, its phenotypic optimum. We first introduce this type of conflict with an illustrative example and assess conditions for maintaining polymorphism for alleles underlying the conflict. We then summarize evidence from our own experiments with Drosophila melanogaster that show substantial genome‐wide sexually antagonistic fitness variation. Finally we discuss evidence from other organisms and some of the ramifications of widespread polymorphism for sexually antagonistic fitness variation.

‘Heads I win, tails you lose’: testing directional alternative hypotheses in ecological and evolutionary research

Whenever experiments make a priori predictions about the direction of change in some parameter, one-tailed test statistics offer a potentially large gain in power over the corresponding two-tailed test. This gain is rarely used in ecology and evolution because of (1) the belief that one-tailed procedures are unavailable for most statistical tests and (2) an inherent dilemma in one-tailed tests: how do we handle large parameter changes in the unanticipated direction? The first problem is a misconception, whereas the second is easily resolved by recognizing that one- and two-tailed tests are simply extremes in a continuum of testing options.

Disruptive selection on habitat preference and the evolution of reproductive isolation: a simulation study

There has been a wide diversity of theoretical work on the genetic mechanisms that promote speciation under sympatric (non-allopatric) conditions (see Thoday and Gibson, 1970; Bush, 1975; Endler, 1977; White, 1978; Futuyma and Mayer, 1980; Templeton, 1981 for review). The conclusion from this work is that sympatric speciation is genetically possible but it is not clear whether or not it has played a major role in the generation of species under natural conditions. Assessing the evolutionary importance of sympatric speciation awaits the identification of those environmental circumstances that are most likely to promote the process. Here I suggest that environmental conditions which produce disruptive selection on habitat preference represent a special case in which sympatric speciation is particularly likely to occur. By habitat preference I mean any tendency of an organism to become non-randomly associated with a particular spatial and/ or temporal part of an environment.

Are all sex chromosomes created equal

Three principal types of chromosomal sex determination are found in nature: male heterogamety (XY systems, as in mammals), female heterogamety (ZW systems, as in birds), and haploid phase determination (UV systems, as in some algae and bryophytes). Although these systems share many common features, there are important biological differences between them that have broad evolutionary and genomic implications. Here we combine theoretical predictions with empirical observations to discuss how differences in selection, genetic properties and transmission uniquely shape each system. We elucidate how the differences among these systems can be exploited to gain insights about general evolutionary processes, genome structure, and gene expression. We suggest directions for research that will greatly increase our general understanding of the forces driving sex-chromosome evolution in diverse organisms.

Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster.

Theory predicts that males will benefit when they bias their mating effort towards females of higher reproductive potential, and that this discrimination will increase as males become more resource limited. We conducted a series of experiments to test these predictions in a laboratory population of the fruitfly, Drosophila melanogaster. In this species, courtship and copulation have significant costs to males, and females vary greatly in fecundity, which is positively associated with body size. When given a simultaneous choice between small and large virgin females, males preferentially mated with larger, more fecund, females. Moreover, after males had recently mated they showed a stronger preference for larger females. These results suggest that male D. melanogaster adaptively allocate their mating effort in response to variation in female quality and provide some of the first support for the theoretical prediction that male stringency in mate choice increases as resources become more limiting.

Population-based resequencing of experimentally evolved populations reveals the genetic basis of body size variation in Drosophila melanogaster.

Body size is a classic quantitative trait with evolutionarily significant variation within many species. Locating the alleles responsible for this variation would help understand the maintenance of variation in body size in particular, as well as quantitative traits in general. However, successful genome-wide association of genotype and phenotype may require very large sample sizes if alleles have low population frequencies or modest effects. As a complementary approach, we propose that population-based resequencing of experimentally evolved populations allows for considerable power to map functional variation. Here, we use this technique to investigate the genetic basis of natural variation in body size in Drosophila melanogaster. Significant differentiation of hundreds of loci in replicate selection populations supports the hypothesis that the genetic basis of body size variation is very polygenic in D. melanogaster. Significantly differentiated variants are limited to single genes at some loci, allowing precise hypotheses to be formed regarding causal polymorphisms, while other significant regions are large and contain many genes. By using significantly associated polymorphisms as a priori candidates in follow-up studies, these data are expected to provide considerable power to determine the genetic basis of natural variation in body size.