Interaction between natural and sexual selection during the evolution of mate recognition

The interaction between natural and sexual selection is central to many theories of how mate choice and reproductive isolation evolve, but their joint effect on the evolution of mate recognition has not, to my knowledge, been investigated in an evolutionary experiment. Natural and sexual selection were manipulated in interspecific hybrid populations of Drosophila to determine their effects on the evolution of a mate recognition system comprised of cuticular hydrocarbons (CHCs). The effect of natural selection in isolation indicated that CHCs were costly for males and females to produce. The effect of sexual selection in isolation indicated that females preferred males with a particular CHC composition. However, the interaction between natural and sexual selection had a greater effect on the evolution of the mate recognition system than either process in isolation. When natural and sexual selection were permitted to operate in combination, male CHCs became exaggerated to a greater extent than in the presence of sexual selection alone, and female CHCs evolved against the direction of natural selection. This experiment demonstrated that the interaction between natural and sexual selection is critical in determining the direction and magnitude of the evolutionary response of the mate recognition system.     

Genetic constraints and the evolution of display trait sexual dimorphism by natural and sexual selection

The evolution of sexual dimorphism involves an interaction between sex-specific selection and a breakdown of genetic constraints that arise because the two sexes share a genome. We examined genetic constraints and the effect of sex-specific selection on a suite of sexually dimorphic display traits in Drosophila serrata. Sexual dimorphism varied among nine natural populations covering a substantial portion of the species range. Quantitative genetic analyses showed that intersexual genetic correlations were high because of autosomal genetic variance but that the inclusion of X-linked effects reduced genetic correlations substantially, indicating that sex linkage may be an important mechanism by which intersexual genetic constraints are reduced in this species. We then explored the potential for both natural and sexual selection to influence these traits, using a 12-generation laboratory experiment in which we altered the opportunities for each process as flies adapted to a novel environment. Sexual dimorphism evolved, with natural selection reducing sexual dimorphism, whereas sexual selection tended to increase it overall. To this extent, our results are consistent with the hypothesis that sexual selection favors evolutionary divergence of the sexes. However, sex-specific responses to natural and sexual selection contrasted with the classic model because sexual selection affected females rather than males.     

Interactions between the sexes: new perspectives on sexual selection and reproductive isolation

Understanding the processes underlying the origin of new species is a fundamental problem in evolutionary research. Whilst it has long been recognised that closely related taxa often differ markedly in reproductive characteristics, only relatively recently has sexual selection been evoked as a key promoter of speciation through its ability to generate reproductive isolation (RI). Sexual selection potentially can influence the probability that individuals from the same or different populations will reproduce successfully since it shapes precisely those traits involved in mating and reproduction. If reproductive characters diverge along different trajectories, then sexual selection can impact on the evolution of reproductive barriers operating both before and after mating. In this perspective, we consider some new advances in our understanding of the coevolution of male and female sexual signals and receptors and suggest how these developments may provide heretofore neglected insights into the mechanisms by which isolating barriers may emerge. Specifically, we explore how selfish genetic elements (SGEs) can mediate pre- and post-copulatory mate choice, thereby influencing gene flow and ultimately population divergence; we examine evidence from studies of intracellular sperm–egg interactions and propose that intracellular gametic incompatibilities may arise after sperm entry into the egg, and thus contribute to RI; we review findings from genomic studies demonstrating rapid, adaptive evolution of reproductive genes in both sexes and discuss whether such changes are causal in determining RI or simply associated with it; and finally, we consider genetic, developmental and functional mechanisms that might constrain reproductive trait diversification, thereby limiting the scope for reproductive barriers to arise via sexual selection. We hope to stimulate work that will further the understanding of the role sexual selection plays in generating RI and ultimately speciation.     

Natural and sexual selection on a plumage signal of status and on morphology in house sparrows,Passer domesticus

Temporal patterns of natural and sexual selection on male badge size and body traits were studied in a population of house sparrows, Passer domesticus. Badge size was a heritable trait as revealed by a significant father-son regression. Survival during autumn dispersal and winter was not related to badge size or body traits in yearling male house sparrows. Badges that signal dominance status were affected positively by directional selection for mating. Adult male house sparrows suffered an opposing selection pressure on badge size during autumn. Contrary to males, female house sparrows did not experience significant directional or stabilizing selection on any body trait. Directional sexual selection on male badge size due to female choice moves male sparrows away from their survival optimum. Opposing directional natural selection on badge size due to autumn mortality caused by predation maintains a stable badge size.     

Interactions between natural selection, recombination and gene density in the genes of Drosophila

In Drosophila, as in many organisms, natural selection leads to high levels of codon bias in genes that are highly expressed. Thus codon bias is an indicator of the intensity of one kind of selection that is experienced by genes and can be used to assess the impact of other genomic factors on natural selection. Among 13,000 genes in the Drosophila genome, codon bias has a slight positive, and strongly significant, association with recombination--as expected if recombination allows natural selection to act more efficiently when multiple linked sites segregate functional variation. The same reasoning leads to the expectation that the efficiency of selection, and thus average codon bias, should decline with gene density. However, this prediction is not confirmed. Levels of codon bias and gene expression are highest for those genes in an intermediate range of gene density, a pattern that may be the result of a tradeoff between the advantages for gene expression of close gene spacing and disadvantages arising from regulatory conflicts among tightly packed genes. These factors appear to overlay the more subtle effect of linkage among selected sites that gives rise to the association between recombination rate and codon bias.     

Pseudogene evolution and natural selection for a compact genome

Pseudogenes are nonfunctional copies of protein-coding genes that are presumed to evolve without selective constraints on their coding function. They are of considerable utility in evolutionary genetics because, in the absence of selection, different types of mutations in pseudogenes should have equal probabilities of fixation. This theoretical inference justifies the estimation of patterns of spontaneous mutation from the analysis of patterns of substitutions in pseudogenes. Although it is possible to test whether pseudogene sequences evolve without constraints for their protein-coding function, it is much more difficult to ascertain whether pseudogenes may affect fitness in ways unrelated to their nucleotide sequence. Consider the possibility that a pseudogene affects fitness merely by increasing genome size. If a larger genome is deleterious--for example, because of increased energetic costs associated with genome replication and maintenance--then deletions, which decrease the length of a pseudogene, should be selectively advantageous relative to insertions or nucleotide substitutions. In this article we examine the implications of selection for genome size relative to small (1-400 bp) deletions, in light of empirical evidence pertaining to the size distribution of deletions observed in Drosophila and mammalian pseudogenes. There is a large difference in the deletion spectra between these organisms. We argue that this difference cannot easily be attributed to selection for overall genome size, since the magnitude of selection is unlikely to be strong enough to significantly affect the probability of fixation of small deletions in Drosophila.     

Reversed plumage ontogeny in a female hummingbird: implications for the evolution of iridescent colours and sexual dichromatism

In polygynous birds, bright plumage is typically more extensive in the sexually competitive males and develops at or after sexual maturity. These patterns, coupled with the importance of male plumage in sexual displays, fostered the traditional hypothesis that bright plumages and sexual dichromatism develop through the actions of sexual selection on males. This view remains problematic for hummingbirds, all of which are polygynous, because their bright iridescent plumages are also important non-sexual signals associated with dominance at floral nectar sources. Here I show that female amethyst-throated sunangels [ Heliangelus amethysticollis (d'Orbigny & Lafresnaye)], moult from an immature plumage with an iridescent gorget to an adult plumage with a non-iridescent gorget. This 'reversed' ontogeny contradicts the notion that iridescent plumage has a sexual function because sexual selection in polygynous birds should be lowest among non-reproductive immature females. Moreover, loss of iridescent plumage in adult females indicates that adult sexual dichromatism in H. amethysticollis is due in large part to changes in female ontogeny. I suggest that both the ontogeny and sexual dichromatism evolved in response to competition for nectar.     

Oxidative damage in relation to a female plumage badge: evidence for signalling costs

Badges of status may be controlled by costs derived from increased aggression from dominant individuals. This cost could be translated into elevated metabolic levels and a concomitant disruption of oxidative balance. Some females in Iberian pied flycatcher Ficedula hypoleuca populations exhibit a white forehead patch similar to that exhibited by all males in this species, functioning in aggressive interactions between females when competing for breeding sites. To test if social stress imposes costs on signalling, we painted white patches on females without natural patches (NP) and compared them with females with natural control (NU). We also over-painted the natural patch in other females (FP) and compared to females with control natural patches (FU). We obtained for the whole sample of females data on reproductive investment, morphology and oxidative damage measured by blood malondialdehydes (MDA), and in a subsample of females variables related to parental care during incubation and the early nestling stage. FP and FU did not differ significantly in any variable which negates an effect of paint itself. However, NP females showed significant higher levels of MDA than NU females when controlling for breeding success for the whole sample, and for female incubation attendance for the parental care subsample. When including the four treatments, there was a significant interaction between the paint treatment and the presence/absence of badges before the experiment when controlling for the significant negative effect of incubation attendance on MDA. Addition of a badge to females without one leads to increased oxidative damage possibly mediated by social control. Badges of status in female pied flycatchers may operate as badges of oxidative status.     

Adaptations to sexual selection and sexual conflict: insights from experimental evolution and artificial selection

Artificial selection and experimental evolution document natural selection under controlled conditions. Collectively, these techniques are continuing to provide fresh and important insights into the genetic basis of evolutionary change, and are now being employed to investigate mating behaviour. Here, we focus on how selection techniques can reveal the genetic basis of post-mating adaptations to sexual selection and sexual conflict. Alteration of the operational sex ratio of adult Drosophila over just a few tens of generations can lead to altered ejaculate allocation patterns and the evolution of resistance in females to the costly effects of elevated mating rates. We provide new data to show how male responses to the presence of rivals can evolve. For several traits, the way in which males responded to rivals was opposite in lines selected for male-biased, as opposed to female-biased, adult sex ratio. This shows that the manipulation of the relative intensity of intra- and inter-sexual selection can lead to replicable and repeatable effects on mating systems, and reveals the potential for significant contemporary evolutionary change. Such studies, with important safeguards, have potential utility for understanding sexual selection and sexual conflict across many taxa. We discuss how artificial selection studies combined with genomics will continue to deepen our knowledge of the evolutionary principles first laid down by Darwin 150 years ago.     

An experimental demonstration of Fisher's principle: evolution of sexual proportion by natural selection.

Most sexually reproducing species have sexual proportions around 1:1. This major biological phenomenon remained unexplained until 1930, when FISHER proposed that it results from a mechanism of natural selection. Here we report the first experimental test of his model that obeys all its assumptions. We used a naturally occurring X-Y meiotic drive system--the sex-ratio trait of Drosophila mediopunctat--to generate female-biased experimental populations. As predicted by FISHER, these populations evolved toward equal sex proportions due to natural selection, by accumulation of autosomal alleles that direct the parental reproductive effort toward the rare sex. Classical Fisherian evolution is a rather slow mechanism: despite a very large amount of genetic variability, the experimental populations evolved from 16% of males to 32% of males in 49 generations and would take 330 generations (29 years) to reach 49%. This slowness has important implications for species potentially endangered by skewed sexual proportions, such as reptiles with temperature sex determination.     

Macroevolutionary patterns of bumblebee body size: detecting the interplay between natural and sexual selection

Bumblebees and other eusocial bees offer a unique opportunity to analyze the evolution of body size differences between sexes. The workers, being sterile females, are not subject to selection for reproductive function and thus provide a natural control for parsing the effects of selection on reproductive function (i.e., sexual and fecundity selection) from other natural selection. Using a phylogenetic comparative approach, we explored the allometric relationships among queens, males, and workers in 70 species of bumblebees (Bombus sp.). We found hyperallometry in thorax width for males relative to workers, indicating greater evolutionary divergence of body size in males than in sterile females. This is consistent with the hypothesis that selection for reproductive function, most probably sexual selection, has caused divergence in male size among species. The slope for males on workers was significantly steeper than that for queens on workers and the latter did not depart from isometry, providing further evidence of greater evolutionary divergence in male size than female size, and no evidence that reproductive selection has accelerated divergence of females. We did not detect significant hyperallometry when male size was regressed directly on queen size and our results thus add the genus Bombus to the increasing list of clades that have female-larger sexual size dimorphism and do not conform to Rensch's rule when analyzed according to standard methodology. Nevertheless, by using worker size as a common control, we were able to demonstrate that bumblee species do show the evolutionary pattern underlying Rensch's rule, that being correlated evolution of body size in males and females, but with greater evolutionary divergence in males.     

Mating games: cultural evolution and sexual selection

In this paper, we argue that mating games, a concept that denotes cultural practices characterized by a competitive element and an ornamental character, are essential drivers behind the emergence and maintenance of human cultural practices. In order to substantiate this claim, we sketch out the essential role of the game’s players and audience, as well as the ways in which games can mature and turn into relatively stable cultural practices. After outlining the life phase of mating games – their emergence, rise, maturation, and possible eventual decline – we go on to argue that participation in these games (in each phase) does make sense from an adaptationist point of view. The strong version of our theory which proposes that all cultural practices are, or once were, mating games, allows us to derive a set of testable predictions for the fields of archaeology, economics, and psychology.     

Bayesian natural selection and the evolution of perceptual systems

In recent years, there has been much interest in characterizing statistical properties of natural stimuli in order to better understand the design of perceptual systems. A fruitful approach has been to compare the processing of natural stimuli in real perceptual systems with that of ideal observers derived within the framework of Bayesian statistical decision theory. While this form of optimization theory has provided a deeper understanding of the information contained in natural stimuli as well as of the computational principles employed in perceptual systems, it does not directly consider the process of natural selection, which is ultimately responsible for design. Here we propose a formal framework for analysing how the statistics of natural stimuli and the process of natural selection interact to determine the design of perceptual systems. The framework consists of two complementary components. The first is a maximum fitness ideal observer, a standard Bayesian ideal observer with a utility function appropriate for natural selection. The second component is a formal version of natural selection based upon Bayesian statistical decision theory. Maximum fitness ideal observers and Bayesian natural selection are demonstrated in several examples. We suggest that the Bayesian approach is appropriate not only for the study of perceptual systems but also for the study of many other systems in biology.     

Uncorrelated evolution between vocal and plumage coloration traits in the trogons: a comparative study

The costs of bird song incurred in a diversity of ways may result in trade‐offs in the production and maintenance of elaborate plumage ornaments. In this paper, we examine evolutionary trade‐offs between acoustic and visual signalling in trogon birds (Trogonidae). Using multiple regressions with phylogenetically independent contrasts, we found that interspecific variation in male plumage coloration was not significantly predicted by song traits (reduced by PCA) or altitude. Although plumage coloration is expected to decrease with increases in song elaboration, both groups of variables were not related. Given that song and plumage coloration traits are likely targets of sexual selection, we also examined their relationships with sexual plumage dimorphism. We found that male carotenoid‐derived coloration was positively related to sexual plumage dimorphism, suggesting that sexual selection on male carotenoid‐derived coloration may be stronger than on melanin‐ or structurally based coloration, or than on acoustic traits. Comparative studies on other bird families accounting for the effects of phylogeny as well as environmental covariates are required to test the generality of our findings in trogons.     

A sexual selection model for hominid evolution

The following paper develops a sexual selection model for the evolution of bipedal locomotion, canine reduction, brain enlargement, language and higher intelligence. The model involves an expansion of Darwin’s ideas about human evolution based on recent elaborations of sexual selection theory. Modern notions about intrasexual competition and female and male choice and their ecological correlates are summarized along with a new model for the role of sexual selection in speciation. Rapid evolution of bipedal locomotion as a male adaptation for nuptial feeding of females is proposed as a model for ape-hominid divergence through sexual selection; canine reduction is attributed to selection for associated epigamic displays. The analogy with male specialization through sexual selection speciation in hamadryas baboons is noted. Subsequent changes in female reproductive physiology are attributed to female competition for increased male parental investment during the time of early Homo andHomo erectus. The origin of higher intellectual and language abilities inHomo sapiens is attributed to male competition through technology and rule production to control resources and females; intellectual abilities involved in social manipulation are attributed to female competition for male parental investment and maintenance of polyandry. The course of hominid evolution is characterized as involving a trend from a promiscuous mating system toward increasing intensity of adaptations for male control of females, and by increasing intensity of female adaptation to maintain male parental investment while circumventing male control.     

On the moulding of senescence by natural selection in sexual and partly sexual populations

Under a wide variety of dynamic environmental conditions, natural selection appears to favor reproductive investment in a sexually produced offspring, carrying only half of the mother’s genes, over the investment in an asexually produced offspring, genetically identical to her. It is maintained that the same environmental conditions must affect the evolutionary cost and benefit of an investment in the prolongation of one’s own life versus an investment in sexual reproduction, in favor of the latter. The effects of different environmental conditions on the division of resources among sexual reproduction, asexual reproduction and prolongation of life are studied.