Age-dependent female responses to a male ejaculate signal alter demographic opportunities for selection

A central tenet of evolutionary explanations for ageing is that the strength of selection wanes with age. However, data on age-specific expression and benefits of sexually selected traits are lacking—particularly for traits subject to sexual conflict. We addressed this by using as a model the responses of Drosophila melanogaster females of different ages to receipt of sex peptide (SP), a seminal fluid protein transferred with sperm during mating. SP can mediate sexual conflict, benefitting males while causing fitness costs in females. Virgin and mated females of all ages showed significantly reduced receptivity in response to SP. However, only young virgin females also showed increased egg laying; hence, there was a narrow demographic window of maximal responses to SP. Males gained significant ‘per mating’ fitness benefits only when mating with young females. The pattern completely reversed in matings with older females, where SP transfer was costly. The overall benefits of SP transfer (hence opportunity for selection) therefore reversed with female age. The data reveal a new example of demographic variation in the strength of selection, with convergence and conflicts of interest between males and ageing females occurring over different facets of responses to a sexually antagonistic trait.     

Sexual isolation evolves faster than hybrid inviability in a diverse and sexually dimorphic genus of fish (Percidae: Etheostoma)

Abstract .Theory predicts that sexual (or behavioral) isolation will be the first form of reproductive isolation to evolve in lineages characterized by sexual selection. Here I directly compare the rate of evolution of sexual isolation with that of hybrid inviability in a diverse and sexually dimorphic genus of freshwater fish. The magnitude of both sexual isolation and hybrid inviability were quantified for multiple pairs of allopatric species. Rates of evolution were inferred by comparing genetic distances of these species pairs with the magnitude of each form of reproductive isolation: the slope of the regression of genetic distance on the magnitude of reproductive isolation represents the rate of evolution. Of the two forms of isolation, the magnitude of sexual isolation exhibited the steeper slope of regression, indicating that sexual isolation will tend to evolve to completion earlier than hybrid inviability, strictly as a by-product of evolution in geographically isolated populations. Additional evidence from the literature is used to qualitatively compare rates of evolution of sexual isolation with that of other forms of reproductive isolation. Preliminary comparisons support the prediction that sexual isolation will evolve more rapidly than other forms. Because Etheostoma is characterized by striking sexual dimorphism, these results are consistent with the hypothesis that sexual selection for exaggerated mate-recognition characters causes the relatively rapid evolution of sexual isolation.     

Reproductive isolation among allopatric Drosophila montana populations

An outstanding goal in speciation research is to trace the mode and tempo of the evolution of barriers to gene flow. Such research benefits from studying incipient speciation, in which speciation between populations has not yet occurred, but where multiple potential mechanisms of reproductive isolation (RI: i.e., premating, postmating‐prezygotic (PMPZ), and postzygotic barriers) may act. We used such a system to investigate these barriers among allopatric populations of Drosophila montana. In all heteropopulation crosses we found premating (sexual) isolation, which was either symmetric or asymmetric depending on the population pair compared. Postmating isolation was particularly strong in crosses involving males from one of the study populations, and while sperm were successfully transferred, stored, and motile, we experimentally demonstrated that the majority of eggs produced were unfertilized. Thus, we identified the nature of a PMPZ incompatibility. There was no evidence of intrinsic postzygotic effects. Measures of absolute and relative strengths of pre‐ and postmating barriers showed that populations differed in the mode and magnitude of RI barriers. Our results indicate that incipient RI among populations can be driven by different contributions of both premating and PMPZ barriers occurring between different population pairs and without the evolution of postzygotic barriers.     

Strong premating reproductive isolation drives incipient speciation in Mimulus aurantiacus

Determining which forms of reproductive isolation have the biggest impact on the process of divergence is a major goal of speciation research. These barriers are often divided into those that affect the potential for hybridization (premating isolation), and those that occur after mating (postmating isolation), and much debate has surrounded the relative importance of these categories. Within the species Mimulus aurantiacus, red‐ and yellow‐flowered ecotypes occur in the southwest corner of California, and a hybrid zone occurs where their ranges overlap. We show that premating barriers are exclusively responsible for isolation in this system, with both ecogeographic and pollinator isolation contributing significantly to total isolation. Postmating forms of reproductive isolation have little or no impact on gene flow, indicating that hybrids likely contribute to introgression at neutral loci. Analysis of molecular variation across thousands of restriction‐site associated DNA sequencing (RAD‐seq) markers reveals that the genomes of these taxa are largely undifferentiated. However, structure analysis shows that these taxa are distinguishable genetically, likely due to the impact of loci underlying differentiated adaptive phenotypes. These data exhibit the power of divergent natural selection to maintain highly differentiated phenotypes in the face of gene flow during the early stages of speciation.     

The evolution of premating isolation: local adaptation and natural and sexual selection against hybrids

Although reinforcement is ostensibly driven by selection against hybrids, there are often other components in empirical cases and theoretical models of reinforcement that may contribute to premating isolation. One of these components is local adaptation of a trait used in mate choice. I use several different comparisons to assess the roles that local adaptation and selection against hybrids may play in reinforcement models. Both numerical simulations of exact recursion equations and analytical weak selection approximations are employed. I find that selection against hybrids may play a small role in driving preference evolution in a reinforcement model where the mating cue is separate from loci causing hybrid incompatibilities. When females have preferences directly for purebreds of their own population, however, selection against hybrids can play a large role in premating isolation evolution. I present some situations in which this type of selection is likely to exist. This work also illustrates shortfalls of using a weak selection approach to address questions about reinforcement.     

BEYOND REINFORCEMENT: THE EVOLUTION OF PREMATING ISOLATION BY DIRECT SELECTION ON PREFERENCES AND POSTMATING, PREZYGOTIC INCOMPATIBILITIES

Abstract The evolution of premating isolation after secondary contact is primarily considered in the guise of reinforcement, which relies on low hybrid fitness as the driving force for mating preference divergence. Here I consider two additional forces that may play a substantial role in the adaptive evolution of premating isolation, direct selection on preferences and indirect selection against postmating, prezygotic incompatibilities. First, I argue that a combination of ecological character displacement and sensory bias can cause direct selection on preferences that results in the pattern of reproductive character displacement. Both analytical and numerical methods are then used to demonstrate that, as expected from work in single populations, such direct selection will easily overwhelm indirect selection due to low hybrid fitness as the primary determinant of preference evolution. Second, postmating, prezygotic incompatibilities are presented as a driving force in the evolution of premating isolation. Two classes of these mechanisms, those increasing female mortality after mating but before producing offspring and those reducing female fertility, are shown to be identical in their effects on preference divergence. Analytical and numerical techniques are then used to demonstrate that postmating, prezygotic factors may place strong selection on preference divergence. These selective forces are shown to be comparable if not greater than those produced by the low fitness of hybrids.     

Variation in male‐built nest volume with nesting‐support quality,colony, and egg production in whiskered terns

Nest building can represent an energetically costly activity for a variety of animal taxa. Besides, the determinants of within‐species variation in the design of nests, notably with respect to natural and sexual selection, are still insufficiently documented. Based on an observational study, we examined the influence of nesting conditions (nesting‐support quality, colony, laying date, and year) on male‐built nest volume and also its potential role as a postmating sexually selected display in the whiskered tern Chlidonias hybrida. This tern species is a monogamous colonial bird with obligate biparental care breeding on aquatic vegetation. Hence, large nesting platforms are expected to be a selective advantage because they would better withstand adverse environmental conditions and provide a secure structure for eggs. Nest size may also serve as a postmating sexual trait, and variation in egg production would be positively associated with nest size. We found that nest volume was adjusted to different environmental cues. A positive relationship was found between nest volume and nesting‐support quality, indicating that the leaf density of white waterlily is essential for nest stability. Variation in nest volume was not correlated to colony size but varied among colonies and years. Male‐built nest volume was also positively associated with mean egg volume per clutch but not with clutch size. The fitness consequences of building a large nest are yet to be studied, and additional investigations are recommended to better understand whether the activity of males early during breeding season (e.g., nest building and courtship feeding performance) really serves as postmating sexually selected signals.     

Divergence in style length and pollen size leads to a postmating‐prezygotic reproductive barrier among populations of Silene latifolia

A central tenet of speciation research is the need to identify reproductive isolating barriers. One approach to this line of research is to identify the phenotypes that lead to reproductive isolation. Several studies on flowering plants have shown that differences in style length contribute to reproductive isolation between species, leading us to consider whether style length could act as a reproductive barrier among populations of a single species. This could occur if style length varied sufficiently and pollen size covaried with style length. Populations of Silene latifolia exhibit variation in flower size, including style length, that is negatively correlated with annual precipitation. We show that this divergence in style length has a genetic basis and acts as a reproductive barrier: males from small‐flowered populations produced relatively small pollen grains that were poor at fertilizing ovules when crossed to females from large‐flowered populations, leading to a significant reduction in seed production. Manipulating the distance pollen tubes had to travel revealed that this failure was purely mechanical and not the result of other incompatibilities. These results show that style length acts as a postmating‐prezygotic reproductive barrier and indicate a potential link between ecotypic differentiation and reproductive isolation within a species.     

Natural selection hampers divergence of reproductive traits in a seed beetle

Speciation is thought to often result from indirect selection for reproductive isolation. This will occur when reproductive traits that cause reproductive isolation evolve (i) as a by‐product of natural selection on traits with which they are genetically correlated or (ii) as an indirect result of diversifying sexual selection. Here, we use experimental evolution to study the degree of divergent evolution of reproductive traits by manipulating the intensity of natural and sexual selection in replicated selection lines of seed beetles. Following 40 generations of selection, we assayed the degree of divergent evolution of reproductive traits between replicate selection lines experiencing the same selection regime. The evolution of reproductive traits was significantly divergent across selection lines within treatments. The evolution of reproductive traits was both slower and, more importantly, significantly less divergent among lines experiencing stronger directional natural selection. This suggests that reproductive traits did not evolve as an indirect by‐product of adaptation. We discuss several ways in which natural selection may hamper divergent evolution among allopatric populations.     

Initial stages of reproductive isolation in two species of the endangered Sonoran topminnow

Long-term geographic isolation can result in reproductive incompatibilities due to forces such as mutation, genetic drift, and differential selection. In the Sonoran topminnow, molecular genetic studies of mtDNA, microsatellites, and MHC genes have shown that the endangered Gila and Yaqui topminnows are substantially different, suggesting that divergence took place approximately two million years ago. Here we examined hybrid crosses and backcrosses between these two allopatric taxa to evaluate the accumulation of postmating barriers to reproduction. These results are then compared with results from a previous study where male topminnows were shown to mate assortatively with conspecific females. Despite their preference for conspecific mates, both types of interspecific crosses successfully produced offspring. There was evidence of reduced hybrid fitness, including smaller mean brood size and male-biased sex ratio, for some classes of backcrosses. Brood sizes and interbrood intervals varied significantly when hybrids were subdivided into different cross categories. Our results illustrate the importance of distinctly defining hybrid classes in studies of reproductive isolation. To our knowledge, this is the first such detailed evolutionary analysis in endangered fish taxa.