Sexual selection drives the coevolution of male and female reproductive traits in Peromyscus mice

When females mate with multiple partners within a single reproductive cycle, sperm from rival males may compete for fertilization of a limited number of ova, and females may bias the fertilization of their ova by particular sperm. Over evolutionary timescales, these two forms of selection shape both male and female reproductive physiology when females mate multiply, yet in monogamous systems, post-copulatory sexual selection is weak or absent. Here, we examine how divergent mating strategies within a genus of closely related mice, Peromyscus, have shaped the evolution of reproductive traits. We show that in promiscuous species, males exhibit traits associated with increased sperm production and sperm swimming performance, and females exhibit traits that are predicted to limit sperm access to their ova including increased oviduct length and a larger cumulus cell mass surrounding the ova, compared to monogamous species. Importantly, we found that across species, oviduct length and cumulus cell density are significantly correlated with sperm velocity, but not sperm count or relative testes size, suggesting that these female traits may have coevolved with increased sperm quality rather than quantity. Taken together, our results highlight how male and female traits evolve in concert and respond to changes in the level of post-copulatory sexual selection.     

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.     

Sperm competition: defining the rules of engagement.

Genetic and cell biological analyses of sperm behavior in the female reproductive tract are providing important clues to the mechanisms of sperm competition, a form of sexual selection that is an important force that shapes reproductive behavior, physiology and morphology in a wide range of species.     

Effects of perinatal polychlorinated biphenyls on adult female rat reproduction: development, reproductive physiology, and second generational effects

Perinatal exposures to endocrine-disrupting chemicals, such as polychlorinated biphenyls (PCBs), can cause latent effects on reproductive function. Here, we tested whether PCBs administered during late pregnancy would compromise reproductive physiology in both the fetally exposed female offspring (F1 generation), as well as in their female offspring (F2 generation). Pregnant Sprague-Dawley rats were treated with the PCB mixture, Aroclor 1221 (A1221; 0, 0.1, 1, or 10 mg/kg), on Embryonic Days 16 and 18. Somatic and reproductive development of F1 and their F2 female offspring were monitored, including ages of eye opening, pubertal landmarks, and serum reproductive hormones. The results showed that low doses of A1221 given during this critical period of neuroendocrine development caused differential effects of A1221 on F1 and F2 female rats. In both generations, litter sex ratio was skewed toward females. In the F1 generation, additional effects were found, including a significant alteration of serum LH in the 1 mg/kg A1221 group. The F2 generation showed more profound alterations, particularly with respect to fluctuations in hormones and reproductive tract tissues across the estrous cycle. On proestrus, the day of the preovulatory GnRH/gonadotropin surge, F2 females whose mothers had been exposed perinatally to A1221 exhibited substantially suppressed LH and progesterone concentrations, and correspondingly smaller uterine and ovarian weights on estrus, compared with F2 descendants of control rats. These latter changes suggest a dysregulation of reproductive physiology. Thus, low levels of exposure to PCBs during late fetal development cause significant effects on the maturation and physiology of two generations of female offspring. These findings have implications for reproductive health and fertility of wildlife and humans.     

Natural selection and glucocorticoid physiology

Glucocorticoid hormones are considered potent modulators of trade‐offs between reproduction and survival. As such, selection should affect glucocorticoid physiology, although relatively little is known about how selection may act on glucocorticoid profiles. In general, the evolution of physiology is less studied and less well understood than morphological or life history traits. Here, we used a long‐term data set from a population of mountain white‐crowned sparrows to estimate natural selection on glucocorticoid profiles. Our study suggests that survival selection favours higher hormone concentrations for multiple components of glucocorticoid physiology (both baseline and stress‐induced glucocorticoid levels). Fecundity selection varies depending on the component of hypothalamic–pituitary–adrenal physiology; greater reproductive output was associated with higher baseline glucocorticoid levels, but lower stress‐induced glucocorticoid levels. Additionally, the selection gradient was greater for glucocorticoids than for a morphological trait (wing length). These results support the hypothesis that stress‐induced glucocorticoids increase survival over reproduction within a wild population (the CORT‐trade‐off hypothesis). Taken together, these results add to our knowledge of how selection operates on physiological traits and also provide an evolutionary and ecological perspective on several key open issues in the field of glucocorticoid physiology.     

Arsenic abrogates the estrogen-signaling pathway in the rat uterus

Background  

Arsenic, a major pollutant of water as well as soil, is a known endocrine disruptor, and shows adverse effects on the female reproductive physiology. However, the exact molecular events leading to reproductive dysfunctions as a result of arsenic exposure are yet to be ascertained. This report evaluates the effect and mode of action of chronic oral arsenic exposure on the uterine physiology of mature female albino rats.     

Neonatal neural organizing effects of exogenous corticosteroids on sexual differentiation of the brain in the female rat

Testosterone, deoxycorticosterone, or vehicle was administered neonatally to female Long-Evans rats. Parameters expressing the reproductive physiology and behavior of the adult animals were studied. It was found that neonatal administration of testosterone produced the expected "defeminization" and "masculinization" of the brain, affecting both the reproductive behavior and cyclicity of these females. In contrast, neonatal administration of the adrenal steroid did not affect cyclicity although it "defeminized" and "masculinized" sexual behavior, albeit to a lesser degree than testosterone. The results suggest a dichotomy in the neuroregulation of reproductive physiology and sexual behavior.     

Sexual selection and speciation in mammals,butterflies and spiders

Recently refined evolutionary theories propose that sexual selection and reproductive conflict could be drivers of speciation. Male and female reproductive optima invariably differ because the potential reproductive rate of males almost always exceeds that of females: females are selected to maximize mate 'quality', while males can increase fitness through mate 'quantity'. A dynamic, sexually selected conflict therefore exists in which 'competitive' males are selected to override the preference tactics evolved by 'choosy' females. The wide variation across taxa in mating systems therefore generates variance in the outcome of intrasexual conflict and the strength of sexual selection: monandry constrains reproductive heterozygosity and allows female choice to select and maintain particular (preferred) genes; polyandry promotes reproductive heterozygosity and will more likely override female choice. Two different theories predict how sexual selection might influence speciation. Traditional ideas indicate that increased sexual selection (and hence conflict) generates a greater diversity of male reproductive strategies to be counteracted by female mate preferences, thus providing elevated potentials for speciation as more evolutionary avenues of male-female interaction are created. A less intuitively obvious theory proposes that increased sexual selection and conflict constrains speciation by reducing the opportunities for female mate choice under polyandry. We use a comparative approach to test these theories by investigating whether two general measures of sexual selection and the potential for sexual conflict have influenced speciation. Sexual size dimorphism (across 480 mammalian genera, 105 butterfly genera and 148 spider genera) and degree of polyandry (measured as relative testes size in mammals (72 genera) and mating frequency in female butterflies (54 genera)) showed no associations with the variance in speciosity. Our results therefore show that speciation occurs independently of sexual selection.     

Competitive PCR reveals the complexity of postcopulatory sexual selection in Teleogryllus commodus

The outcome of mate choice depends on complex interactions between males and females both before and after copulation. Although the competition between males for access to mates and premating choice by females are relatively well understood, the nature of interactions between cryptic female choice and male sperm competition within the female reproductive tract is less clear. Understanding the complexity of postcopulatory sexual selection requires an understanding of how anatomy, physiology and behaviour mediate sperm transfer and storage within multiply mated females. Here we use a newly developed molecular technique to directly quantify mixed sperm stores in multiple mating females of the black field cricket, Teleogryllus commodus. In this species, female postcopulatory choice is easily observed and manipulated as females delay the removal of the spermatophore in favour of preferred males. Using twice‐mated females, we find that the proportion of sperm in the spermatheca attributed to the second male to mate with a female (S₂) increases linearly with the time of spermatophore attachment. Moreover, we show that the insemination success of a male increases with its attractiveness and decreases with the size of the female. The effect of male attractiveness in this context suggests a previously unknown episode of mate choice in this species that reinforces the sexual selection imposed by premating choice and conflicts with the outcome of postmating male harassment. Our results provide some of the clearest evidence yet for how sperm transfer and displacement in multiply mated females can lead directly to cryptic female choice, and that three distinct periods of sexual selection operate in black field crickets.     

Sexual selection is a form of social selection

Social selection influences the evolution of weapons, ornaments and behaviour in both males and females. Thus, social interactions in both sexual and non-sexual contexts can have a powerful influence on the evolution of traits that would otherwise appear to be detrimental to survival. Although clearly outlined by West-Eberhard in the early 1980s, the idea that social selection is a comprehensive framework for the study of ornaments and weapons has largely been ignored. In West-Eberhard's view, sexual selection is a form of social selection-a concept supported by several lines of evidence. Darwin's distinction between natural and sexual selection has been useful, but recent confusion about the limits of sexual selection suggests that some traits are not easily categorized as naturally or sexually selected. Because social selection theory has much to offer the current debates about both sexual selection and reproductive competition in females, it is sometimes viewed, narrowly, to be most useful when considering female roles. However, social selection theory encompasses much more than female reproductive competition. Our goal here was to provide that broader perspective.     

Optical coherence tomography for dynamic investigation of mammalian reproductive processes

The biological events associated with mammalian reproductive processes are highly dynamic and tightly regulated by molecular, genetic, and biomechanical factors. Implementation of live imaging in reproductive research is vital for the advancement of our understanding of normal reproductive physiology and for improving the management of reproductive disorders. Optical coherence tomography (OCT) is emerging as a promising tool for dynamic volumetric imaging of various reproductive processes in mice and other animal models. In this review, we summarize recent studies employing OCT-based approaches toward the investigation of reproductive processes in both, males and females. We describe how OCT can be applied to study structural features of the male reproductive system and sperm transport through the male reproductive tract. We review OCT applications for in vitro and dynamic in vivo imaging of the female reproductive system, staging and tracking of oocytes and embryos, and investigations of the oocyte/embryo transport through the oviduct. We describe how the functional OCT approach can be applied to the analysis of cilia dynamics within the male and female reproductive systems. We also discuss the areas of research, where OCT could find potential applications to progress our understanding of normal reproductive physiology and reproductive disorders.     

Postcopulatory sexual selection

The female reproductive tract is where competition between the sperm of different males takes place, aided and abetted by the female herself. Intense postcopulatory sexual selection fosters inter-sexual conflict and drives rapid evolutionary change to generate a startling diversity of morphological, behavioural and physiological adaptations. We identify three main issues that should be resolved to advance our understanding of postcopulatory sexual selection. We need to determine the genetic basis of different male fertility traits and female traits that mediate sperm selection; identify the genes or genomic regions that control these traits; and establish the coevolutionary trajectory of sexes.     

Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection

Genes whose products are involved in reproduction include some of the fastest-evolving genes found within the genomes of several organisms. Drosophila has long been used to study the function and evolutionary dynamics of genes thought to be involved in sperm competition and sexual conflict, two processes that have been hypothesized to drive the adaptive evolution of reproductive molecules. Several seminal fluid proteins (Acps) made in the Drosophila male reproductive tract show evidence of rapid adaptive evolution. To identify candidate genes in the female reproductive tract that may be involved in female-male interactions and that may thus have been subjected to adaptive evolution, we used an evolutionary bioinformatics approach to analyze sequences from a cDNA library that we have generated from Drosophila female reproductive tracts. We further demonstrate that several of these genes have been subjected to positive selection. Their expression in female reproductive tracts, presence of signal sequences/transmembrane domains, and rapid adaptive evolution indicate that they are prime candidates to encode female reproductive molecules that interact with rapidly evolving male Acps.     

Sexual selection in a lekking bird: the relative opportunity for selection by female choice and male competition

Leks are classic models for studies of sexual selection due to extreme variance in male reproductive success, but the relative influence of intrasexual competition and female mate choice in creating this skew is debatable. In the lekking lance-tailed manakin (Chiroxiphia lanceolata), these selective episodes are temporally separated into intrasexual competition for alpha status and female mate choice among alpha males that rarely interact. Variance in reproductive success between status classes of adult males (alpha versus non-alpha) can therefore be attributed to male-male competition whereas that within status largely reflects female mate choice. This provides an excellent opportunity for quantifying the relative contribution of each of these mechanisms of sexual selection to the overall opportunity for sexual selection on males (I males). To calculate variance in actual reproductive success, we assigned genetic paternity to 92.3% of 447 chicks sampled in seven years. Reproduction by non-alphas was rare and apparently reflected status misclassifications or opportunistic copulations en route to attaining alpha status rather than alternative mating strategies. On average 31% (range 7-44%, n=6 years) of the total I males was due to variance in reproductive success between alphas and non-alphas. Similarly, in a cohort of same-aged males followed for six years, 44-58% of the total I males was attributed to variance between males of different status. Thus, both intrasexual competition for status and female mate choice among lekking alpha males contribute substantially to the potential for sexual selection in this species.     

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.     

A measure of sexual selection in hermaphroditic animals: parentage skew and the opportunity for selection

The role of sexual selection in shaping the mating system of hermaphrodites is currently widely accepted. However, a quantification of the intensity of sexual selection in hermaphroditic animals has never been accomplished. We evaluated the opportunity for sexual selection for both the female and the male functions in the simultaneous outcrossing hermaphrodite Ophryotrocha diadema by measuring focal hermaphrodites' paternal and maternal offspring in experimental replicated monogamous and promiscuous populations, using genetic markers to estimate paternity. Opportunity for sexual selection for each of the two sexual functions was quantified by means of the Crow's index, i.e. the ratio of variance in progeny number to the squared mean number of progeny. In addition, the extent to which the reproductive success was shared among competing individuals was estimated by means of the Nonacs's B index. We documented that the strength of selection on the male and female function in hermaphrodites with external fertilization depends on the reproductive context. Under a promiscuous regime, hermaphrodites have higher opportunities for selection for both the male and the female function than under the monogamous regime. Moreover, the reproductive skew for the female function becomes greater than that for the male function, moving from monogamy to promiscuity. In our model system, allocation to one sexual function is opposed by any degree of allocation to the other, indicating that sex-specific patterns of selection operate in this model species.     

Reproductive aspects and storage of semen in camelidae

The characteristics of male and female reproductive tracts and reproductive physiology in camelids are described. An account is given on methods of collection, characteristics and storage of semen, and fertility after artificial insemination (AI) with fresh, liquid-stored and frozen-thawed lamoid and camel semen.     

Sexually antagonistic selection on primate size

Abstract Male intrasexual selection in haplorhine primates has previously been shown to increase male size and to a lesser degree also female size. I address the following questions: (1) why does female size increase when the selection is on males, and (2) why does female size not increase to the same extent as that of males. The potential for correlational selection on females through increased resource competition was analysed with independent contrasts analyses. No such effect was found, nor did matched pairs comparisons reveal females to increase in size because of selection to bear larger male offspring. Instead further matched pairs analyses revealed higher female postpartum investment, as indicated by a longer lactation period, in more sexually selected species, also after correcting for body weight. Concerning the second question, independent contrast analyses showed that large size has had negative effects on female reproductive rate across the primate order. Matched‐pairs analyses on haplorhines revealed that females of species in more polygynous clades have lower reproductive rates than females of species in less polygynous clades. This is also true after the effects of body weight are removed. These results, both when correcting for body weight and when not, suggest that sexual selection has shifted female size from one favouring female lifetime fecundity to one favouring male success in competition. This depicts antagonistic selection pressures on female size and a trade‐off for females between the ecologically optimal size of their foremothers and the larger size that made their forefathers successful.     

Melatonin-pineal relationships in female golden hamsters.

Light deprivation by blinding in female hamsters was followed by a regression of the reproductive organs, an elevation of pituitary LH concentration and a depression of pituitary prolactin levels. Pinealectomy negated almost completely the effects of light deprivation on the neuroendocrine-reproductive axis. Weekly subcutaneous implants of a melatonin:beeswax pellet completely prevented the pineal gland from inhibiting reproductive physiology in blinded hamsters. The findings suggest that melatonin is not pineal antigonadotrophic factor in female golden hamsters. Melatonin implanted hamsters also had higher than normal levels of plasma prolactin.     

Diversity-enhancing selection acts on a female reproductive protease family in four subspecies of Drosophila mojavensis

Protein components of the Drosophila male ejaculate are critical modulators of reproductive success, several of which are known to evolve rapidly. Recent evidence of adaptive evolution in female reproductive tract proteins suggests this pattern may reflect sexual selection at the molecular level. Here we explore the evolutionary dynamics of a five-paralog gene family of female reproductive proteases within geographically isolated subspecies of Drosophila mojavensis. Remarkably, four of five paralogs show exceptionally low differentiation between subspecies and unusually structured haplotypes that suggest the retention of old polymorphisms. These gene genealogies are accompanied by deviations from neutrality consistent with diversifying selection. While diversifying selection has been observed among the reproductive molecules of mammals and marine invertebrates, our study provides the first evidence of this selective regime in any Drosophila reproductive protein, male or female.