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PubMed2001

Adaptive design, selective history, and women's sexual motivations.

I have discussed an ongoing program of research designed to examine the nature of specific sexual selection pressures that have played a role in the evolution of human mating. I have suggested that the evidence tentatively be interpreted as consistent with the existence of female preferences for traits that indicate good genes. Nonetheless, more research is needed before definitive conclusions can be reached. At the outset, I discussed several points about the application of adaptationism to an understanding of human behavior. First, special-design arguments are often critical to evolutionary explanations. Special design is not only evidence that natural selection has been at work, it can also reveal the nature of selection pressures that have shaped the organism. Second, special design often cannot be readily "read off" the observed phenotype. A convincing special-design argument may require a coordinated, coherent explanation (a nomological network; Cronbach & Meehl, 1955) of multiple and varied observations. Third, observations that are "strange coincidences" if one's explanation is not correct, but expected if one's explanation is correct, are particularly informative pieces of evidence. The research on sexual selection illustrates these points. We have attempted to provide evidence for special design in females for preferring men who demonstrate developmental precision for the benefit of obtaining good genes. We can point to no one piece of evidence that directly demonstrates this special design. The explanation that women possess special design for preferring men who possess good genes in certain mating contexts (such as extra-pair sex), however, does provide a coherent account of a wide range of findings. At least one of these findings--that women prefer the scent of symmetrical men only when the probability of conception is high--was expected by this explanation, but has no obvious alternate explanation and hence appears to be a strange, peculiar coincidence if this explanation is wrong. By no means do we have a full and complete story here. The nomological network can and should be expanded in a number of ways and, thereby, the argument for special design tightened. Whether or not the special-design argument ultimately holds up to further scrutiny, however, I would like to think that our efforts to establish it have importantly contributed to an understanding of human mating.

Biological Evolution↗

PubMed2006

Contrasting evolution of expression differences in the testis between species and subspecies of the house mouse.

Regulatory changes in genes involved in reproduction are thought to be prime targets for divergence during speciation, since they are expected to play an important role in sexual selection and sexual conflict. We used microarray analysis of RNA from different wild populations of house mouse subspecies (including Mus m. musculus, Mus m. domesticus, and Mus m. castaneus) and from the sister species Mus spretus to test this assumption. A comparison of expression divergence in brain, liver/kidney, and testis shows a major difference in the evolutionary dynamics of testis-related genes. While the comparison between species confirms an excess in divergence in testis genes, we find that all comparisons between subspecies yield only a very small number of genes with significantly different expression levels in the testis. These results suggest that the early phase of the speciation process may not be driven by regulatory changes in genes that are potential targets of sexual selection, and that the divergence in these genes is only established during a later phase of the speciation process.

Animals↗

PubMed1987

The evolution of plant reproductive characters; sexual versus natural selection.

The rôle of sexual selection in the evolution of plant reproductive characters has become a widely discussed topic among plant population biologists. For many reproductive characters, it is difficult to distinguish whether sexual selection or natural selection has been the more important force. We propose a definition of sexual selection for cosexual species and critically review the topic of sexual selection in plants. The emphasis of the chapter is on the evolution of plant reproductive characters, rather than on the issue of whether certain phenomena should be classified as sexual or natural selection. We do, however, argue that the category of sexual selection should not include the phenomena of inbreeding depression, genetically based self-incompatibility systems controlled by one or a few loci, or the effects of wide crossing and specific combining ability. We then discuss the available information on pollen competition and progeny quality, fruit and seed abortion, and the rôle of pollinator attraction in male and female fertility.

Biological Evolution↗

PubMed2006

Live fast, die young: trade-offs between fitness components and sexually antagonistic selection on weaponry in Soay sheep.

Males are predicted to compete for reproductive opportunities, with sexual selection driving the evolution of large body size and weaponry through the advantage they confer for access to females. Few studies have explored potential trade-offs of investment in secondary sexual traits between different components of fitness or tested for sexually antagonistic selection pressures. These factors may provide explanations for observed polymorphisms in both form and quality of secondary sexual traits. We report here an analysis of selection on horn phenotype in a feral population of Soay sheep (Ovis aries) on the island of Hirta, St. Kilda, Scotland. Soay sheep display a phenotypic polymorphism for horn type with males growing either normal or reduced (scurred) horns, and females growing either normal, scurred, or no (polled) horns; further variation in size exists within horn morphs. We show that horn phenotype and the size of the trait displayed is subject to different selection pressures in males and females, generating sexually antagonistic selection. Furthermore, there was evidence of a trade-off between breeding success and longevity in normal-horned males, with both the normal horn type and larger horn size being associated with greater annual breeding success but reduced longevity. Therefore, selection through lifetime breeding success was not found to act upon horn phenotype in males. In females, a negative association of annual breeding success within the normal-horned phenotype did not result in a significant difference in lifetime fitness when compared to scurred individuals, as no significant difference in longevity was found. However, increased horn size within this group was negatively associated with breeding success and longevity. Females without horns (polled) suffered reduced longevity and thus reduced lifetime breeding success relative the other horn morphs. Our results therefore suggest that trade-offs between different components of fitness and antagonistic selection between the sexes may maintain genetic variation for secondary sexual traits within a population.

Animals↗

PubMed2006

Sexual conflict and the evolution of female preferences for indicators of male quality.

Males and females have opposing interests when it comes to the honesty of signals used in mate choice. The existence of this sexual conflict has long been acknowledged, but its consequences have not been fully investigated. By applying adaptive dynamics methods and individual-based computer simulations to a standard model for good-genes sexual selection, we show that sexual conflict over condition-dependent signaling can prevent the handicap process from ever attaining an evolutionary equilibrium. We outline the parameter conditions and properties of the underlying genetics conducive to nonequilibrium behavior and discuss the potential of such behavior to explain the elaboration and frequent phylogenetic loss of sexually selected traits. We also evaluate its consequences for well-established insights of sexual selection theory previously shown to apply when female mating preference and male ornament expression do converge on stable equilibrium levels. Contrary to equilibrium expectation, a continual change of condition-dependent signaling enables the evolution of a costly preference for a pure epistatic indicator and the evolution of preferences for redundant signals or a large number of independent ornaments. We thus conclude that seemingly general results of sexual selection theory, insofar as these are based on equilibrium considerations, do not extend to cases where nonequilibrium behavior occurs.

Adaptation, Biological↗

PubMed2005

The evolution of male traits in social insects.

Pair formation in social insects mostly happens early in adult life and away from the social colony context, which precludes promiscuity in the usual sense. Termite males have continuous sperm production, but males of social Hymenoptera have fixed complements of sperm, except for a few species that mate before female dispersal and show male-fighting and lifelong sperm production. We develop an evolutionary framework for testing sexual selection and sperm competition theory across the advanced eusocial insects (ants, wasps, bees, termites) and highlight two areas related to premating sexual selection (sexual dimorphism and male mate number) that have remained understudied and in which considerable progress can be achieved with relatively simple approaches. We also infer that mating plugs may be relatively common, and we review further possibilities for postmating sexual selection, which gradually become less likely in termite evolution, but for which eusocial Hymenoptera provide unusual opportunities because they have clonal ejaculates and store viable sperm for up to several decades.

Animals↗

PubMed2005

Allometry for sexual size dimorphism: testing two hypotheses for Rensch's rule in the water strider Aquarius remigis.

Within any given clade, male size and female size typically covary, but male size often varies more than female size. This generates a pattern of allometry for sexual size dimorphism (SSD) known as Rensch's rule. I use allometry for SSD among populations of the water strider Aquarius remigis (Hemiptera, Gerridae) to test the hypothesis that Rensch's rule evolves in response to sexual selection on male secondary sexual traits and an alternative hypothesis that it is caused by greater phenotypic plasticity of body size in males. Comparisons of three populations reared under two temperature regimes are combined with an analysis of allometry for genital and somatic components of body size among 25 field populations. Contrary to the sexual-selection hypothesis, genital length, the target of sexual selection, shows the lowest allometric slope of all the assayed traits. Instead, the results support a novel interpretation of the differential-plasticity hypothesis: that the traits most closely associated with reproductive fitness (abdomen length in females and genital length in males) are "adaptively canalized." While this hypothesis is unlikely to explain Rensch's rule among species or higher clades, it may explain widespread patterns of intraspecific variation in SSD recently documented for many insect species.

Animals↗

PubMed2007

Male mating preferences pre-date the origin of a female trait polymorphism in an incipient species complex of Lake Victoria cichlids.

Disruptive sexual selection on colour patterns has been suggested as a major cause of diversification in the cichlid species flock of Lake Victoria. In Neochromis omnicaeruleus, a colour and sex determination polymorphism is associated with a polymorphism in male and female mating preferences. Theoretical work on this incipient species complex found conditions for rapid sympatric speciation by selection on sex determination and sexual selection on male and female colour patterns, under restrictive assumptions. Here we test the biological plausibility of a key assumption of such models, namely, the existence of a male preference against a novel female colour morph before its appearance in the population. We show that most males in a population that lacks the colour polymorphism exhibit a strong mating preference against the novel female colour morph and that reinforcement is not a likely explanation for the origin of such male preferences. Our results show that a specific condition required for the combined action of selection on sex determination and sexual selection to drive sympatric speciation is biologically justified. Finally, we suggest that Lake Victoria cichlids might share an ancestral female recognition scheme, predisposing colour monomorphic populations/species to similar evolutionary pathways leading to divergence of colour morphs in sympatry.

Animals↗

PubMed2000

Lifetime selection on adult body size and components of body size in a waterstrider: opposing selection and maintenance of sexual size dimorphism.

Sexual size dimorphism (SSD), the difference in body size between males and females, is common in almost all taxa of animals and is generally assumed to be adaptive. Although sexual selection and fecundity selection alone have often been invoked to explain the evolution of SSD, more recent views indicate that the sexes must experience different lifetime selection pressures for SSD to evolve and be maintained. We estimated selection acting on male and female adult body size (total length) and components of body size in the waterstrider Aquarius remigis during three phases of life history. Opposing selection pressures for overall body size occurred in separate episodes of fitness for females in both years and for males in one year. Specific components of body size were often the targets of the selection on overall body size. When net adult fitness was estimated by combining each individual's fitnesses from all episodes, we found stabilizing selection in both sexes. In addition, the net optimum overall body size of males was smaller than that of females. However, even when components of body size had experienced opposing selection pressures in individual episodes, no components appeared to be under lifetime stabilizing selection. This is the first evidence that contemporary selection in a natural population acts to maintain female size larger than male size, the most common pattern of SSD in nature.

Animals↗

PubMed2005

Correlational selection leads to genetic integration of body size and an attractive plumage trait in dark-eyed juncos.

When a trait's effect on fitness depends on its interaction with other traits, the resultant selection is correlational and may lead to the integration of functionally related traits. In relation to sexual selection, when an ornamental trait interacts with phenotypic quality to determine mating success, correlational sexual selection should generate genetic correlations between the ornament and quality, leading to the evolution of honest signals. Despite its potential importance in the evolution of signal honesty, correlational sexual selection has rarely been measured in natural populations. In the dark-eyed junco (Junco hyemalis), males with experimentally elevated values of a plumage trait (whiteness in the tail or "tail white") are more attractive to females and dominant in aggressive encounters over resources. We used restricted maximum-likelihood analysis of a long-term dataset to measure the heritability of tail white and two components of body size (wing length and tail length), as well as genetic correlations between pairs of these traits. We then used multiple regression to assess directional, quadratic, and correlational selection as they acted on tail white and body size via four components of lifetime fitness (juvenile and adult survival, mating success, and fecundity). We found a positive genetic correlation between tail white and body size (as measured by wing length), which indicates past correlational selection. Correlational selection, which was largely due to sexual selection on males, was also found to be currently acting on the same pair of traits. Larger males with whiter tails sired young with more females, most likely due to a combination of female choice, which favors males with whiter tails, and male-male competition, which favors both tail white and larger body size. To our knowledge, this is the first study to show both genetic correlations between sexually selected traits and currently acting correlational sexual selection, and we suggest that correlational sexual selection frequently may be an important mechanism for maintaining the honesty of sexual signals.

Animals↗

PubMed2006

Phylogenetic analyses of dimorphism in primates: evidence for stronger selection on canine size than on body size.

Phylogenetic comparative methods were used to analyze the consequences of sexual selection on canine size and canine size dimorphism in primates. Our analyses of previously published body mass and canine size data revealed that the degree of sexual selection is correlated with canine size dimorphism, as well as with canine size in both sexes, in haplorhine but not in strepsirrhine primates. Consistent with these results, male and female canine size was found to be highly correlated in all primates. Since canine dimorphism and canine size in both sexes in haplorhines were found to be not only related to mating system but also to body size and body size dimorphism (characters which are also subject to or the result of sexual selection), it was not apparent whether the degree of canine dimorphism is the result of sexual selection on canine size itself, or whether canine dimorphism is instead a consequence of selection on body size, or vice versa. To distinguish among these possibilities, we conducted matched-pairs analyses on canine size after correcting for the effects of body size. These tests revealed significant effects of sexual selection on relative canine size, indicating that canine size is more important in haplorhine male-male competition than body size. Further analyses showed, however, that it was not possible to detect any evolutionary lag between canine size and body size, or between canine size dimorphism and body size dimorphism. Additional support for the notion of special selection on canine size consisted of allometric relationships in haplorhines between canine size and canine size dimorphism in males, as well as between canine size dimorphism and body size dimorphism. In conclusion, these analyses revealed that the effects of sexual selection on canine size are stronger than those on body size, perhaps indicating that canines are more important than body size in haplorhine male-male competition.

Animals↗

PubMed2004

Reproductive consequences of population divergence through sexual conflict.

Sexual-selection research increasingly focuses on reproductive conflicts between the sexes. Sexual conflict, divergent evolutionary interests of males and females, can cause rapid antagonistic coevolution of reproductive traits and is a potentially powerful speciation engine. This idea has theoretical and comparative support but remains controversial. Recent experimental evidence from Sepsis cynipsea indicates that populations with greater sexual conflict diverged more quickly; females were less likely to mate with males from other populations when flies had evolved under high levels of sexual conflict. The consequences of this divergence have not been addressed, so here we assess two female fitness surrogates after 44 generations of evolving (and diverging) under three different levels of sexual conflict. Longevity after copulation was negatively associated with the degree of sexual conflict under which flies evolved, and housing females with males also reduced female longevity. Female lifetime reproductive success (LRS) also tended to decrease with increasing conflict. However, there was evidence of either sexual-selection fitness benefits at intermediate levels of sexual selection and conflict or inbreeding depression in the smallest populations (those with the lowest levels of conflict). Nevertheless, the results indicate that there can be a fitness load associated with sexual selection and support claims that sexual conflict can lead to reproductive isolation.

Animals↗

PubMed2005

Hamilton and Zuk meet heterozygosity? Song repertoire size indicates inbreeding and immunity in song sparrows (Melospiza melodia).

Hamilton and Zuk's influential hypothesis of parasite-mediated sexual selection proposes that exaggerated secondary sexual ornaments indicate a male's addictive genetic immunity to parasites. However, genetic correlated of ornaments and immunity have rarely been explicitly identified. Evidence supporting Hamilton and Zuk's hypothesis has instead been gathered by looking for positive phenotypic correlations between ornamentation and immunity; such correlations are assumed to reflect causal, addictive relationships between these traits. We show that in a song sparrows, Melospiza melodia, male's song repertoire size, a secondary sexual trait, increased with his cell-mediated immune response (CMI) to an experimental challenge. However, this phenotypic correlation could be explained because both repertoire size and CMI declined with a male's inbreeding level. Repertoire size therefore primarily indicated a male's relative heterozygosity, a non-addictive genetic predictor of immunity. Caution may therefore be required when interpreting phenotypic correlations as support for Hamilton and Zuk's addictive model of sexual selection. However, our results suggest that female song sparrows choosing with large repertoires would on average acquire more outbred and therefore more heterozygous mates. Such genetic dominance effects on ornamentation are likely to influence evolutionary trajectories of female choice, and should be explicitly incorporated into genetic models of sexual selection.

Animals↗

PubMed1987

The cost of sex.

The potential costs of sex can be divided into two large categories. The first category consists of costs that are not derived from anisogamy, and includes costs associated with recombination, with delay of synthesis at the cellular level (cellular-mechanical cost), and with fertilization. The second large category of costs is derived from anisogamy. Specific costs include the cost of genome dilution (cost of males) and the cost of sexual selection. The cost of genome dilution applies to sexual females in anisogamous organisms because the female provides cytoplasm and reserve materials to support the male genome as well as her own genome. The cost of sexual selection is caused by loss of fitness through selection resulting from sexual competition, or through dual phenotypic specialization of a single species as a result of sexual selection. All factors contributing to the cost of sex apply potentially to a broad spectrum of organisms. However, numerous mechanisms reduce the realized cost of sex to a level far below the potential cost. The potential cost is likely to be highest in small organisms, but the realized cost among these organisms is reduced greatly by intermittent sexuality. The realized cost of sex tends to increase with size and complexity among organisms because of increasing commitment to sex with increasing size. Increasing commitment to sex is required by the lower reproductive rates and consequently lower rates of adaptation in larger organisms, which would put such organisms at a disadvantage in relation to smaller organisms were it not for increasing commitment to sexual recombination in larger organisms. Comparable commitment to sex is not possible in smaller organisms because such organisms have a higher potential cost of sex, which maintains among them a lower limit on the frequency of sex.

Animals↗

PubMed2003

Costs and benefits of evolving under experimentally enforced polyandry or monogamy.

Reproduction has classically been viewed as a predominantly cooperative process. However, over the last 20 years this concept has steadily yielded ground to one of continual conflict in which the interests of the sexes are typically discordant. Within this framework, males and females are seen to be locked into a perpetual arms race, each adaptation by one sex promoting the evolution of countermeasures in the other sex. However, under strict genetic monogamy, the interests of the sexes become congruent, and hence antagonistic coevolution does not occur. We subjected the fly Sepsis cynipsea, a species with conspicuous sexual conflict, to experimentally enforced monogamy or polyandry for 29 generations and evaluated the microevolutionary consequences. We found that there were longevity costs to females consistent with sexually antagonistic coevolution. However, our measure of female fitness, offspring emergence, did not differ between treatments, even though life-history characters such as fertility and fecundity did. Results are discussed in terms of costs and benefits of sexual selection and sexual conflict.

Animals↗

PubMed2006

The quantitative genetic basis of polyandry in the parasitoid wasp, Nasonia vitripennis.

Understanding the evolution of female multiple mating (polyandry) is crucial for understanding sexual selection and sexual conflict. Despite this interest, little is known about its genetic basis or whether genetics influences the evolutionary origin or maintenance of polyandry. Here, we explore the quantitative genetic basis of polyandry in the parasitoid wasp Nasonia vitripennis, a species in which female re-mating has been observed to evolve in the laboratory. We performed a quantitative genetic experiment on a recently collected population of wasps. We found low heritabilities of female polyandry (re-mating frequency after 18 h), low heritability of courtship duration and a slightly higher heritability of copulation duration. However, the coefficients of additive genetic variance for these traits were all reasonably large (CV(A)>7.0). We also found considerable dam effects for all traits after controlling for common environment, suggesting either dominance or maternal effects. Our work adds to the evidence that nonadditive genetic effects may influence the evolution of mating behaviour in Nasonia vitripennis, and the evolution of polyandry more generally.

Animals↗

PubMed2001

Strength and tempo of directional selection in the wild.

Directional selection is a major force driving adaptation and evolutionary change. However, the distribution, strength, and tempo of phenotypic selection acting on quantitative traits in natural populations remain unclear across different study systems. We reviewed the literature (1984-1997) that reported the strength of directional selection as indexed by standardized linear selection gradients (beta). We asked how strong are viability and sexual selection, and whether strength of selection is correlated with the time scale over which it was measured. Estimates of the magnitude of directional selection (absolute value of beta) were exponentially distributed, with few estimates greater than 0.50 and most estimates less than 0.15. Sexual selection (measured by mating success) appeared stronger than viability selection (measured by survival). Viability selection that was measured over short periods (days) was typically stronger than selection measured over longer periods (months and years), but the strength of sexual selection did not vary with duration of selection episodes; as a result, sexual selection was stronger than viability selection over longer time scales (months and years), but not over short time scales (days).

Animals↗

PubMed2001

Genetic evidence for extreme polyandry and extraordinary sex-role reversal in a pipefish.

Due to the phenomenon of male pregnancy, the fish family Syngnathidae (seahorses and pipefishes) has historically been considered an archetypal example of a group in which sexual selection should act more strongly on females than on males. However, more recent work has called into question the idea that all species with male pregnancy are sex-role reversed with respect to the intensity of sexual selection. Furthermore, no studies have formally quantified the opportunity for sexual selection in any natural breeding assemblage of pipefishes or seahorses in order to demonstrate conclusively that sexual selection acts most strongly on females. Here, we use a DNA-based study of parentage in the Gulf pipefish Syngnathus scovelli in order to show that sexual selection indeed acts more strongly on females than on males in this species. Moreover, the Gulf pipefish exhibits classical polyandry with the greatest asymmetry in reproductive roles (as quantified by variances in mating success) between males and females yet documented in any system. Thus, the intensity of sexual selection on females in pipefish rivals that of any other taxon yet studied.

Animals↗