Male genotype affects female longevity in Drosophila melanogaster

Several recent studies suggest that interactions with conspecific males can reduce the longevity of female Drosophila melanogaster or support the idea that male and female fitness components are involved in antagonistic interactions. Here we report that males from third-chromosome isogenic lines demonstrated significant genetic variation in male reproductive performance and in the longevity of their mates. Increased male performance was marginally significantly associated with one measure of increased female survival rate. However, there was no indication of tradeoffs or negative correlations between male reproductive success and female survival. We discuss alternative hypotheses for the cause of the induced variation in female longevity.     

The sexual selection continuum

The evolution of mate choice for genetic benefits has become the tale of two hypotheses: Fisher's 'run-away' and 'good genes', or viability indicators. These hypotheses are often pitted against each other as alternatives, with evidence that attractive males sire more viable offspring interpreted as support for good genes and with a negative or null relationship between mating success of sons and other components of fitness interpreted as favouring the Fisher process. Here, we build a general model of female choice for indirect benefits that captures the essence of both the 'Fisherian' and 'good-genes' models. All versions of our model point to a single process that favours female preference for males siring offspring of high reproductive value. Enhanced mating success and survival are therefore equally valid genetic benefits of mate choice, but their relative importance varies depending on female choice costs. The relationship between male attractiveness and survival may be positive or negative, depending on life-history trade-offs and mating skew. This relationship can change sign in response to increased costliness of choice or environmental change. Any form of female preference is subject to self-reinforcing evolution, and any relationship (or lack thereof) between male display and offspring survival is inevitably an indicator of offspring reproductive values. Costly female choice can be maintained with or without higher offspring survival.     

Migration and the evolution of sexual dichromatism: evolutionary loss of female coloration with migration among wood-warblers

The mechanisms underlying evolutionary changes in sexual dimorphism have long been of interest to biologists. A striking gradient in sexual dichromatism exists among songbirds in North America, including the wood-warblers (Parulidae): males are generally more colourful than females at northern latitudes, while the sexes are similarly ornamented at lower latitudes. We use phylogenetically controlled comparative analysis to test three non-mutually exclusive hypotheses for the evolution of sexual dichromatism among wood-warblers. The first two hypotheses focus on the loss of female coloration with the evolution of migration, either owing to the costs imposed by visual predators during migration, or owing to the relaxation of selection for female social signalling at higher latitudes. The third hypothesis focuses on whether sexual dichromatism evolved owing to changes in male ornamentation as the strength of sexual selection increases with breeding latitude. To test these hypotheses, we compared sexual dichromatism to three variables: the presence of migration, migration distance, and breeding latitude. We found that the presence of migration and migration distance were both positively correlated with sexual dichromatism, but models including breeding latitude alone were not strongly supported. Ancestral state reconstruction supports the hypothesis that the ancestral wood-warblers were monochromatic, with both colourful males and females. Combined, these results are consistent with the hypotheses that the evolution of migration is associated with the relaxation of selection for social signalling among females and that there are increased predatory costs along longer migratory routes for colourful females. These results suggest that loss of female ornamentation can be a driver of sexual dichromatism and that social or natural selection may be a stronger contributor to variation in dichromatism than sexual selection.     

Nonadaptive female pursuit of extrapair copulations can evolve through hitchhiking

Mounting evidence has indicated that engaging in extrapair copulations (EPCs) might be maladaptive or detrimental to females. It is unclear why such nonadaptive female behavior evolves. In this study, we test two hypotheses about the evolution of female EPC behavior using population genetic models. First, we find that both male preference for allocating extra effort to seek EPCs and female pursuit behavior without costs can be maintained and remain polymorphic in a population via frequency‐dependent selection. However, both behaviors cannot evolve when females with pursuit behavior suffer from a decline in male parental care. Second, we present another novel way in which female pursuit behavior can evolve; indirect selection can act on this behavior through a ratchet‐like mechanism involving oscillating linkage disequilibria between the target EPC pursuit locus and two other loci determining male mate choice and a female sexual signal. Although the overall positive force of such indirect selection is relatively weak, our results suggest that it may still play a role in promoting the evolution of female EPC behavior when this behavior is nonadaptive (i.e., it is neutral) or only somewhat maladaptive (e.g., males only occasionally lower parental care when their mates pursue EPCs).     

Persistence of females that produce only female progeny in lepidoptera

In Lepidoptera females that produce only female progeny, can be found in wild populations of at least 11 species. The genetic variation is passed on to each generation of female offspring. If genetically abnormal females produce more female offspring than normal females do and mating is random, then populations containing these abnormal females will have a biased population sex ratio. Unmated females will increase due to the scarcity of males and so the population as a unit will die out. Several possible biological explanations for the persistence of the genetic variation have been proposed. But experiments and observations have not verified those hypotheses. Simulations of Heuch's model (1978), however, have shown that the variation persists if the population is distributed, in patches and there is dispersal among patches, even when insects disperse at random. Abnormal females tend to persist at both low and high migration rates, but the probability of persistence is higher at high migration rates. It has been suggested that abnormal females in a population are an adaptation, but the results of this investigation show that this explanation, may not be plausible.     

The genetic basis of traits regulating sperm competition and polyandry: can selection favour the evolution of good- and sexy-sperm?

The good-sperm and sexy-sperm (GS-SS) hypotheses predict that female multiple mating (polyandry) can fuel sexual selection for heritable male traits that promote success in sperm competition. A major prediction generated by these models, therefore, is that polyandry will benefit females indirectly via their sons' enhanced fertilization success. Furthermore, like classic 'good genes' and 'sexy son' models for the evolution of female preferences, GS-SS processes predict a genetic correlation between genes for female mating frequency (analogous to the female preference) and those for traits influencing fertilization success (the sexually selected traits). We examine the premise for these predictions by exploring the genetic basis of traits thought to influence fertilization success and female mating frequency. We also highlight recent debates that stress the possible genetic constraints to evolution of traits influencing fertilization success via GS-SS processes, including sex-linked inheritance, nonadditive effects, interacting parental genotypes, and trade-offs between integrated ejaculate components. Despite these possible constraints, the available data suggest that male traits involved in sperm competition typically exhibit substantial additive genetic variance and rapid evolutionary responses to selection. Nevertheless, the limited data on the genetic variation in female mating frequency implicate strong genetic maternal effects, including X-linkage, which is inconsistent with GS-SS processes. Although the relative paucity of studies on the genetic basis of polyandry does not allow us to draw firm conclusions about the evolutionary origins of this trait, the emerging pattern of sex linkage in genes for polyandry is more consistent with an evolutionary history of antagonistic selection over mating frequency. We advocate further development of GS-SS theory to take account of the complex evolutionary dynamics imposed by sexual conflict over mating frequency.     

Evolution of the genetic covariance between male and female components of mate recognition: an experimental test

The evolution of a positive genetic correlation between male and female components of mate recognition systems will result as a consequence of assortative mating and, in particular, is central to a number of theories of sexual selection. Although the existence of such genetic correlations has been investigated in a number of taxa, it has yet to be shown that such correlations evolve and whether they may evolve as rapidly as suggested by sexual selection models. In this study, I used a hybridization experiment to disrupt natural mate recognition systems and then observed the subsequent evolutionary dynamics of the genetic correlation between male and female components for 56 generations in hybrids between Drosophila serrata and Drosophila birchii. The genetic correlation between male and female components evolved from 0.388 at generation 5 to 1.017 at generation 37 and then declined to -0.040 after a further 19 generations. These results indicated that the genetic basis of the mate recognition system in the hybrid populations evolved rapidly. The initial rapid increase in the genetic correlation was consistent with the classic assumption that male and female components will coevolve under sexual selection. The subsequent decline in genetic correlation may be attributable to the fixation of major genes, or, alternatively, may be a result of a cyclic evolutionary change in mate recognition.     

FEMALE AND MALE GENETIC EFFECTS ON OFFSPRING PATERNITY: ADDITIVE GENETIC (CO)VARIANCES IN FEMALE EXTRA‐PAIR REPRODUCTION AND MALE PATERNITY SUCCESS IN SONG SPARROWS (MELOSPIZA MELODIA)

Ongoing evolution of polyandry, and consequent extra‐pair reproduction in socially monogamous systems, is hypothesized to be facilitated by indirect selection stemming from cross‐sex genetic covariances with components of male fitness. Specifically, polyandry is hypothesized to create positive genetic covariance with male paternity success due to inevitable assortative reproduction, driving ongoing coevolution. However, it remains unclear whether such covariances could or do emerge within complex polyandrous systems. First, we illustrate that genetic covariances between female extra‐pair reproduction and male within‐pair paternity success might be constrained in socially monogamous systems where female and male additive genetic effects can have opposing impacts on the paternity of jointly reared offspring. Second, we demonstrate nonzero additive genetic variance in female liability for extra‐pair reproduction and male liability for within‐pair paternity success, modeled as direct and associative genetic effects on offspring paternity, respectively, in free‐living song sparrows (Melospiza melodia). The posterior mean additive genetic covariance between these liabilities was slightly positive, but the credible interval was wide and overlapped zero. Therefore, although substantial total additive genetic variance exists, the hypothesis that ongoing evolution of female extra‐pair reproduction is facilitated by genetic covariance with male within‐pair paternity success cannot yet be definitively supported or rejected either conceptually or empirically.     

Female mate choice across spatial scales: influence of lek and male attributes on mating success of blue-crowned manakins

Lekking males compete for females within and among leks, yet female choice is expected to work differently at each of these spatial scales. We used paternity analyses to examine how lek versus male attributes influence mate choice in the blue-crowned manakin Lepidothrix coronata. We tested the hypotheses that females prefer (i) to mate at larger leks where a larger number of potential mates can be assessed, (ii) to mate with unrelated or highly heterozygous males expected to produce high-quality offspring, (iii) to mate with males that display at higher rates, and that (iv) display honestly reflects male genetic quality. Our results show that (i) males at larger leks are not more likely to sire young, although females nesting close to small leks travel further to reach larger leks, (ii) siring males are not less related to females or more heterozygous than expected, (iii) within a lek, high-display males are more likely to sire young, and (iv) both male heterozygosity and display rate increased with lek size, and as a result display does not reliably reflect male genetic quality across leks. We suggest that female mate choice in this species is probably driven by a Fisherian process rather than adaptive genetic benefits.     

Why care? Inferring the evolution of complex social behaviour

Phylogenetic comparative analyses of complex traits often reduce the traits of interests into a single (or a few) component variables. Here, we show that this may be an over‐simplification, because components of a complex trait may evolve independently from each other. Using eight components of parental care in 400 bird species from 89 avian families that represent the relative contribution of male vs. female to a particular type of care, we show that some components evolve in a highly correlated manner, whereas others exhibit low (or no) phylogenetic correlation. Correlations were stronger within types of parental activity (brooding, feeding, guarding) than within stages of the breeding cycle (incubation, prefledging care, post‐fledging care). A phylogenetically corrected cluster analysis identified two groups of parental care components that evolved in a correlated fashion: one group included incubation and brooding, whereas the other group comprised of the remaining components. The two groups of components provide working hypotheses for follow‐up studies to test the underlying genetic, developmental and ecological co‐evolutionary mechanism between male and female care. Furthermore, the components within each group are expected to respond consistently to different ambient and social environments.     

Sexual selection in hermit crabs: a review and outlines of future research

The information currently available on sexual selection in hermit crabs is reviewed to identify the role of males and females before, during and after mating. According to this information, possible mechanisms of male–male competition, female choice and/or sexual conflict are suggested. Important male components that may affect mating success include dragging the female shell, rotations of the female's shell and male cheliped palpations, and male size and/or shell characteristics (species and size). Possible female determinants of male mating/fertilization success include size (as an indicator of egg production capacity), signalling of sexual receptivity to males, delay from mate guarding to copulation and mating duration. Avenues for deeper exploration in males include the role of the number and morphometry of male sexual tubes during sperm transfer, and whether ejaculate size and sperm number can be adjusted with variable situations of sperm competition intensity and risk. In females it would be interesting to investigate the chemical and behavioural mechanisms affecting spermatophore breakage for sperm release and the variable duration from sperm transfer to spawning. Given these possibilities, and that sperm is externally deposited on the female's body but inside her shell (except for those species that do not use shells, e.g. Birgus , or species where shells are rather small and do not cover the body totally, e.g. Parapagurus ), we conclude that hermit crabs are unique subjects for separating male and female effects, particularly with respect to the applicability of current ideas in sexual selection such as female choice and sexual conflict. Some practical ideas are provided to disentangle both hypotheses using these animals.     

Postmarital residence and within-sex genetic diversity among the Urubu-Ka'apor Indians, Brazilian Amazon

The analysis of biologic variation in prehistoric human populations separately by sex has been used as a tool to recover post-marital residential rules. These studies, which focus on the sexual distribution of skeletal traits, assume that the degree of intragroup or intergroup biologic diversity is higher in one sex with regard to unilocality (uxori- or virilocality). Despite a recent attempt to interpret this phenomenon in terms of population genetics (Konigsberg 1988), the main assumption has never been tested in situations in which the real residential practice of an indigenous population is known and in which genetic rather than phenotypic data are available. We investigated the within-group and between-group genetic variability among males and females from 4 villages of an uxorilocal Amazonian tribe, the Urubu-Ka'apor, on the basis of 20 polymorphic loci. The results were only partly concordant with the expected. Individual mean per locus heterozygosities were not different between the sexes, and the analysis of genetic heterogeneity showed similar gene frequencies for males and females in all villages. On the other hand, the intergroup approach detected a level of variation significantly greater among females than among males. The ethnographic evidence shows that three of the four subgroups studied belong to the same gamic unity, with the fourth subgroup belonging to another gamic network. Within-sex differences in intergroup analysis turned out to be more evident; yet, when those 3 villages were investigated separately, the female FST (0.0609) proved to be significantly higher than the male FST (0.0218). Such results suggest that the intergroup analysis is more sensitive to the genetic effects of differential migration rates between the sexes. In prehistoric contexts, therefore, an intergroup genetic approach can provide more reliable grounds for sociocultural inferences.     

Male genotype influences female reproductive investment in Drosophila melanogaster

In many species, males can influence the amount of resources their mates invest in reproduction. Two favoured hypotheses for this observation are that females assess male quality during courtship or copulation and alter their investment in offspring accordingly, or that males manipulate females to invest heavily in offspring produced soon after mating. Here, we examined whether there is genetic variation for males to influence female short-term reproductive investment in Drosophila melanogaster, a species with strong sexual selection and substantial sexual conflict. We measured the fecundity and egg size of females mated to males from multiple isofemale lines collected from populations around the globe. Although these traits were not strongly influenced by the male's population of origin, we found that 22 per cent of the variation in female short-term reproductive investment was attributable to the genotype of her mate. This is the first direct evidence that male D. melanogaster vary genetically in their proximate influence on female fecundity, egg size and overall reproductive investment.     

雌性动物多次交配行为的机制及进化

雌性动物的后代数量不可能超过她的卵子数。在理论上, 一个生殖季节内, 一次或几次交配就足够使雌性所有卵子受精, 最大化其生殖潜能。但与理论预测相反, 许多物种的雌性经常与同一个或多个雄性发生多次交配。交配通常要付出较高的代价, 所以很难理解为什么雌性动物要反复进行多次交配。本文综述了解释此行为的一些适应性和非适应性假说。从获得直接收益和间接收益二个角度介绍了适应性假说。直接收益主要包括求偶喂食和“彩礼”、受精保证、亲代抚育、生殖刺激和护卫交配权等5 个方面。还着重介绍了多次交配对雌性后代的间接遗传受益, 即获得优质基因、提高后代遗传多样性和遗传互补性3 个假说。非适应性假说包括了遗传相关假说和顺从雄性行为假说。     

Why female crested tits copulate repeatedly with the same partner: evidence for the mate assessment hypothesis

That repeated copulation with the same partner within a singlefertile period is beneficial to the male is generally accepted,but why it should be adaptive to the female is controversialand clear evidence supporting any hypothesis is lacking. Hunteret al. (1993) presented seven hypotheses explaining repeatedmating from the female perspective. Four of them are consistentwith the occurrence of male refusal to copulate: females mighttrade copulations for (1) immediate and or (2) future materialbenefits, or use mating as a mechanism for (3) mate-guardingand or (4) mate-assessment. To test these hypotheses in a populationof crested tits Parus cristatus, we collected data on variationin female solicitation rate, proportion of male refusal, andextra-pair paternity. We found that (1) female solicitationrate was independent of male condition, (2) the proportion ofmale refusal was higher in poor-condition males and (3) femalespaired to poor-condition males sought extra pair paternity.These findings agree with predictions stemming from the mateassessment hypothesis. Therefore, it is suggested that, in crestedtits, male response to female copulation solicitation reflectsmale condition and is used by females to assess male quality     

On the origin and evolution of apomixis in Boechera

The genetic mechanisms causing seed development by gametophytic apomixis in plants are predominantly unknown. As apomixis is consistently associated with hybridity and polyploidy, these confounding factors may either (a) be the underlying mechanism for the expression of apomixis, or (b) obscure the genetic factors which cause apomixis. To distinguish between these hypotheses, we analyzed the population genetic patterns of diploid and triploid apomictic lineages and their sexual progenitors in the genus Boechera (Brassicaceae). We find that while triploid apomixis is associated with hybridization, the majority of diploid apomictic lineages are likely the product of intra-specific crosses. We then show that these diploid apomicts are more likely to sire triploid apomictic lineages than conspecific sexuals. Combined with flow cytometric seed screen phenotyping for male and female components of apomixis, our analyses demonstrate that hybridization is an indirect correlate of apomixis in Boechera.     

Survival rates in a natural population of the damselfly Ceriagrion tenellum: effects of sex and female phenotype

1. Ceriagrion tenellum females show genetic colour polymorphism. Androchrome (erythrogastrum) females are brightly (male‐like) coloured while gynochrome females (typica and melanogastrum) show cryptic colouration. 2. Several hypotheses have been proposed to explain the existence of more than one female morph in damselfly populations. The reproductive isolation and intraspecific mimicry hypotheses predict greater survival of gynochrome females, while the density dependent hypothesis predicts no differential survival between morphs. 3. Mature males had greater recapture probability than females while the survival probability was similar for both sexes. Survival and recapture rates were similar for androchrome and gynochrome females. 4. Gynochrome females showed greater mortality or migration rate than androchrome females during the pre‐reproductive period. This result is not predicted by the above hypotheses or by the null hypothesis that colour polymorphism is only maintained by random factors: founder effects, genetic drift, and migration.     

Shape--but not size--codivergence between male and female copulatory structures in Onthophagus beetles

Genitalia are among the fastest evolving morphological traits in arthropods. Among the many hypotheses aimed at explaining this observation, some explicitly or implicitly predict concomitant male and female changes of genital traits that interact during copulation (i.e., lock and key, sexual conflict, cryptic female choice and pleiotropy). Testing these hypotheses requires insights into whether male and female copulatory structures that physically interact during mating also affect each other's evolution and patterns of diversification. Here we compare and contrast size and shape evolution of male and female structures that are known to interact tightly during copulation using two model systems: (a) the sister species O. taurus (1 native, 3 recently established populations) and O. illyricus, and (b) the species-complex O. fracticornis-similis-opacicollis. Partial Least Squares analyses indicated very little to no correlation between size and shape of copulatory structures, both in males and females. Accordingly, comparing shape and size diversification patterns of genitalia within each sex showed that the two components diversify readily--though largely independently of each other--within and between species. Similarly, comparing patterns of divergence across sexes showed that relative sizes of male and female copulatory organs diversify largely independent of each other. However, performing this analysis for genital shape revealed a signature of parallel divergence. Our results therefore suggest that male and female copulatory structures that are linked mechanically during copulation may diverge in concert with respect to their shapes. Furthermore, our results suggest that genital divergence in general, and co-divergence of male and female genital shape in particular, can evolve over an extraordinarily short time frame. Results are discussed in the framework of the hypotheses that assume or predict concomitant evolutionary changes in male and female copulatory organs.     

Divergence of a speciation trait through artificial selection: Insights into constraints,by-product effects and sexual isolation

Speciation and sexual isolation often occur when divergent female mating preferences target male secondary sexual traits. Despite the importance of such male signals, little is known about their evolvability and genetic linkage to other traits during speciation. To answer these questions, we imposed divergent artificial selection for 10 non-overlapping generations on the Inter-Pulse-Interval (IPI) of male courtship songs; which has been previously shown to be a major species recognition trait for females in the Drosophila athabasca species complex. Focusing on one of the species, Drosophila mahican (previously known as EA race), we examined IPI's: (1) rate of divergence, (2) response to selection in different directions, (3) genetic architecture of divergence and (4) by-product effects on other traits that have diverged in the species complex. We found rapid and consistent response for higher IPI but less response to lower IPI; implying asymmetrical constraints. Genetic divergence in IPI differed from natural species in X versus autosome contribution and in dominance, suggesting that evolution may take different paths. Finally, selection on IPI did not alter other components of male songs, or other ecological traits, and did not cause divergence in female preferences, as evidenced by lack of sexual isolation. This suggests that divergence of male courtship song IPI is unconstrained by genetic linkage with other traits in this system. This lack of linkage between male signals and other traits implies that female preferences or ecological selection can co-opt and mould specific male signals for species recognition free of genetic constraints from other traits.     

The evolution of leks through female choice

It is generally acknowledged that female preferences for mating in large groups of displaying males could cause the evolution of leks. Recent hypotheses differ on what selective advantage would accrue to females with such preferences, but they agree on the need for some such advantage if these preferences are to select for larger lek sizes. A model developed here, adapted from models of female preferences for individual male traits, shows that female preferences for larger leks can evolve and be maintained without any direct selective advantage. Like the individual choice models, it also demonstrates a number of arbitrary or non-adaptive features inherent in such systems. Most notably, instead of a single optimal outcome, there may exist a curve of possible equilibria. These equilibria can be stable or unstable depending on the nature of the female preferences.