Monogamous Populations Research Articles

Selection on the Fly: Short-Term Adaptation to an Altered Sexual Selection Regime in Drosophila pseudoobscura.

Experimental evolution studies are powerful approaches to examine the evolutionary history of lab populations. Such studies have shed light on how selection changes phenotypes and genotypes. Most of these studies have not examined the time course of adaptation under sexual selection manipulation, by resequencing the populations' genomes at multiple time points. Here, we analyze allele frequency trajectories in Drosophila pseudoobscura where we altered their sexual selection regime for 200 generations and sequenced pooled populations at 5 time points. The intensity of sexual selection was either relaxed in monogamous populations (M) or elevated in polyandrous lines (E). We present a comprehensive study of how selection alters population genetics parameters at the chromosome and gene level. We investigate differences in the effective population size-Ne-between the treatments, and perform a genome-wide scan to identify signatures of selection from the time-series data. We found genomic signatures of adaptation to both regimes in D. pseudoobscura. There are more significant variants in E lines as expected from stronger sexual selection. However, we found that the response on the X chromosome was substantial in both treatments, more pronounced in E and restricted to the more recently sex-linked chromosome arm XR in M. In the first generations of experimental evolution, we estimate Ne to be lower on the X in E lines, which might indicate a swift adaptive response at the onset of selection. Additionally, the third chromosome was affected by elevated polyandry whereby its distal end harbors a region showing a strong signal of adaptive evolution especially in E lines.

A Comparative Analysis of Adult Sex Ratios in Polygynous and Monogamous Mammal Populations

An inverse density-dependent relationship between abundance and adult sex ratio (ASR, males:female) occurs in some populations of polygynous mammals due to life history differences between the sexes. Male fecundity and survival is dictated by attempts to obtain as many copulations as possible, whereas female fecundity and survival is dictated by resource acquisition. Therefore, females usually acquire forage before males as a result of interspecific scramble competition, particularly when forage becomes more limited at K carrying capacity. This leads to the passive displacement of males in a given area. The common belief is that most monogamous mammal populations exhibit balanced adult sex ratios. The coupling of sexually mature males and females in a population result in this pattern for this mating system. Present literature focuses on primary or secondary sex ratios in mammals or on ASR patterns within individual species. Our goal was to test if expected ASR patterns would be visible across numerous species in both mating systems. We hypothesized we would see an inverse relationship between abundance and ASR across polygynous populations, and no relationship between abundance and ASR across monogamous populations. We extracted time series population data from published literature for 43 populations of 15 different mammal species. Results from our analysis of a linear mixed-effects model were consistent with our hypothesis for polygynous populations, as we found a significant inverse relationship between abundance and ASR. However, our analysis also revealed a significant inverse relationship between abundance and ASR in monogamous populations that was not consistent with our hypothesis. Our findings provide quantitative support for a theoretical model explaining the evolutionary and ecological mechanisms driving a density-dependent relationship between abundance and ASR in polygynous mammals. An investigation into monogamous mammals is needed to assess why some species with this mating system display a density-dependent response in ASR as well.

Metapopulation structure modulates sexual antagonism.

Despite the far‐reaching evolutionary implications of sexual conflict, the effects of metapopulation structure, when populations are subdivided into several demes connected to some degree by migration, on sexual conflict dynamics are unknown. Here, we used experimental evolution in an insect model system, the seed beetle Callosobruchus maculatus, to assess the independent and interacting effects of selection histories associated with mating system (monogamy vs. polygamy) and population subdivision on sexual conflict evolution. We confirm traditional predictions from sexual conflict theory by revealing increased resistance to male harm in females from populations with a history of intense sexual selection (polygamous populations) compared to females from populations with a history of relaxed sexual selection (monogamous populations). However, selection arising from metapopulation structure reversed the classic pattern of sexually antagonistic coevolution and led to reduced resistance in females from polygamous populations. These results underscore that population spatial structure moderates sexual selection and sexual conflict, and more broadly, that the evolution of sexual conflict is contingent on ecological context. The findings also have implications for population dynamics, conservation biology, and biological control.

Mating patterns influence vulnerability to the extinction vortex.

Earth's biodiversity is undergoing mass extinction due to anthropogenic compounding of environmental, demographic and genetic stresses. These different stresses can trap populations within a reinforcing feedback loop known as the extinction vortex, in which synergistic pressures build upon one another through time, driving down population viability. Sexual selection, the widespread evolutionary force arising from competition, choice and reproductive variance within animal mating patterns could have vital consequences for population viability and the extinction vortex: (a) if sexual selection reinforces natural selection to fix 'good genes' and purge 'bad genes', then mating patterns encouraging competition and choice may help protect populations from extinction; (b) by contrast, if mating patterns create load through evolutionary or ecological conflict, then population viability could be further reduced by sexual selection. We test between these opposing theories using replicate populations of the model insect Tribolium castaneum exposed to over 10years of experimental evolution under monogamous versus polyandrous mating patterns. After a 95-generation history of divergence in sexual selection, we compared fitness and extinction of monogamous versus polyandrous populations through an experimental extinction vortex comprising 15 generations of cycling environmental and genetic stresses. Results showed that lineages from monogamous evolutionary backgrounds, with limited opportunities for sexual selection, showed rapid declines in fitness and complete extinction through the vortex. By contrast, fitness of populations from the history of polyandry, with stronger opportunities for sexual selection, declined slowly, with 60% of populations surviving by the study end. The three vortex stresses of (a) nutritional deprivation, (b) thermal stress and (c) genetic bottlenecking had similar impacts on fitness declines and extinction risk, with an overall sigmoid decline in survival through time. We therefore reveal sexual selection as an important force behind lineages facing extinction threats, identifying the relevance of natural mating patterns for conservation management.

Adaptation to monogamy influences parental care but not mating behavior in the burying beetle, Nicrophorus vespilloides.

The mating system is expected to have an important influence on the evolution of mating and parenting behaviors. Although many studies have used experimental evolution to examine how mating behaviors evolve under different mating systems, this approach has seldom been used to study the evolution of parental care. We used experimental evolution to test whether adaptation to different mating systems involves changes in mating and parenting behaviors in populations of the burying beetle, Nicrophorus vespilloides. We maintained populations under monogamy or promiscuity for six generations. This manipulation had an immediate impact on reproductive performance and adult survival. Compared to monogamy, promiscuity reduced brood size and adult (particularly male) survival during breeding. After six generations of experimental evolution, there was no divergence between monogamous and promiscuous populations in mating behaviors. Parents from the promiscuous populations (especially males) displayed less care than parents from the monogamous populations. Our results are consistent with the hypothesis that male care will increase with the certainty of paternity. However, it appears that this change is not associated with a concurrent change in mating behaviors.

Towards a predictive conservation biology: the devil is in the behaviour.

One of the most important challenges in conservation biology is to predict the viability of populations of vulnerable and threatened species. This requires that the demographic stochasticity strongly affecting the ecological and evolutionary dynamics of especially small populations is correctly estimated and modelled. Here, we summarize theoretical evidence showing that the demographic variance in population dynamics is a key parameter determining the probability of extinction and also is directly linked to the magnitude of the genetic drift in the population. The demographic variance is dependent on the mating system, being larger in a polygynous than in monogamous populations. Understanding factors affecting intersexual differences in mating success is therefore essential in explaining variation in the demographic variance. We hypothesize that the strength of sexual selection, for example, quantified by the Bateman gradient, may be a useful predictor of the magnitude of the demographic stochasticity and hence the genetic drift in the population. We provide results from a field study of moose that support this claim. Thus, including central principles from behavioural ecology may increase the reliability of population viability analyses through an improvement of our understanding of factors affecting stochastic influences on population dynamics and evolutionary processes. This article is part of the theme issue 'Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation'.

To save or not to save your family member\u2019s life? Evolutionary stability of self-sacrificing life history strategy in monogamous sexual populations

BackgroundFor the understanding of human nature, the evolutionary roots of human moral behaviour are a key precondition. Our question is as follows: Can the altruistic moral rule “Risk your life to save your family members, if you want them to save your life” be evolutionary stable? There are three research approaches to investigate this problem: kin selection, group selection and population genetics modelling. The present study is strictly based on the last approach.ResultsWe consider monogamous and exogamous families, where at an autosomal locus, dominant-recessive alleles determine the phenotypes in a sexual population. Since all individuals’ survival rate is determined by their altruistic family members, we introduce a new population genetics model based on the mating table approach and adapt the verbal definition of evolutionary stability to genotypes. In general, when the resident is recessive, a homozygote is an evolutionarily stable genotype (ESG), if the number of survivors of the resident genotype of the resident homozygote family is greater than that of non-resident heterozygote survivors of the family of the resident homozygote and mutant heterozygote genotypes. Using the introduced genotype dynamics we proved that in the recessive case ESG implies local stability of the altruistic genotype. We apply our general ESG conditions for self-sacrificing life history strategy when the number of new-born offspring does not depend on interactions within the family and the interactions are additive. We find that in this case our ESG conditions give back Hamilton’s rule for evolutionary stability of the self-sacrificing life history strategy.ConclusionsIn spite of the fact that the kidney transplantations was not a selection factor during the earlier human evolution, nowadays “self-sacrificing” can be observed in the live donor kidney transplantations, when the donor is one of the family members. It seems that selection for self-sacrificing in family produced an innate moral tendency in modulating social cognition in human brain.

Sexual conflict drives male manipulation of female postmating responses in Drosophila melanogaster

In many animals, females respond to mating with changes in physiology and behavior that are triggered by molecules transferred by males during mating. In Drosophila melanogaster, proteins in the seminal fluid are responsible for important female postmating responses, including temporal changes in egg production, elevated feeding rates and activity levels, reduced sexual receptivity, and activation of the immune system. It is unclear to what extent these changes are mutually beneficial to females and males or instead represent male manipulation. Here we use an experimental evolution approach in which females are randomly paired with a single male each generation, eliminating any opportunity for competition for mates or mate choice and thereby aligning the evolutionary interests of the sexes. After >150 generations of evolution, males from monogamous populations elicited a weaker postmating stimulation of egg production and activity than males from control populations that evolved with a polygamous mating system. Males from monogamous populations did not differ from males from polygamous populations in their ability to induce refractoriness to remating in females, but they were inferior to polygamous males in sperm competition. Mating-responsive genes in both the female abdomen and head showed a dampened response to mating with males from monogamous populations. Males from monogamous populations also exhibited lower expression of genes encoding seminal fluid proteins, which mediate the female response to mating. Together, these results demonstrate that the female postmating response, and the male molecules involved in eliciting this response, are shaped by ongoing sexual conflict.

Mate choice intensifies motor signalling in Drosophila

Mate choice has the potential to act on the evolution of motor performance via its direct influence on motor sexual signals. However, studies demonstrating this are rare. Here, we performed an in-depth analysis of Drosophila pseudoobscura courtship song rate, a motor signal under mate choice in this species, and analysed the response of this signal to sexual selection manipulation using experimental evolution. We show that manipulating the opportunity for sexual selection led to changes in song production rate and singing endurance, with males from the polyandrous populations producing faster song rates over longer time periods than males from monogamous populations. We also show that song rate was correlated with estimates of overall courtship vigour. Our results suggest that the action of mate choice on a motor signal has affected male motor performance displayed during courtship. We consider potential selective benefits associated with changes in motor performance, including condition-dependent signalling, and discuss the implications of these results for the study of motor signals under sexual selection.

Evolution of a mating preference for a dual-utility trait used in intrasexual competition in genetically monogamous populations.

The selection pressures by which mating preferences for ornamental traits can evolve in genetically monogamous mating systems remain understudied. Empirical evidence from several taxa supports the prevalence of dual‐utility traits, defined as traits used both as armaments in intersexual selection and ornaments in intrasexual selection, as well as the importance of intrasexual resource competition for the evolution of female ornamentation. Here, we study whether mating preferences for traits used in intrasexual resource competition can evolve under genetic monogamy. We find that a mating preference for a competitive trait can evolve and affect the evolution of the trait. The preference is more likely to persist when the fecundity benefit for mates of successful competitors is large and the aversion to unornamented potential mates is strong. The preference can persist for long periods or potentially permanently even when it incurs slight costs. Our results suggest that, when females use ornaments as signals in intrasexual resource competition, males can evolve mating preferences for those ornaments, illuminating both the evolution of female ornamentation and the evolution of male preferences for female ornaments in monogamous species.

Cultural sexual selection in monogamous human populations.

In humans, both sexes sometimes show peculiar mating preferences that do not appear to increase their fitness either directly or indirectly. As humans may transmit their preferences and target culturally, and these may be artificially modifiable, I develop theoretical models where a preference and/or a trait are culturally transmitted with a restriction of the trait modification. I assume a monogamous population where some individuals fail to find a mate, and this affects the preference and the trait in the next time step. I show that a strong aversion to, or high tolerance of, failed individuals are necessary for the evolution of irrational preferences that neither seek good genes nor any direct benefit. This evolution is more likely to occur when the preference and/or the trait are cultural rather than genetic. These results may partly explain why humans sometimes show mating preferences for exaggerated physical and cultural traits.

Evolution of a mating preference for a dual-utility trait used in intrasexual competition in genetically monogamous populations

Evolution of a mating preference for a dual-utility trait used in intrasexual competition in genetically monogamous populations

Sexual selection shapes development and maturation rates in Drosophila.

Explanations for the evolution of delayed maturity usually invoke trade-offs mediated by growth, but processes of reproductive maturation continue long after growth has ceased. Here, we tested whether sexual selection shapes the rate of posteclosion maturation in the fruit fly Drosophila melanogaster. We found that populations maintained for more than 100 generations under a short generation time and polygamous mating system evolved faster posteclosion maturation and faster egg-to-adult development of males, when compared to populations kept under short generations and randomized monogamy that eliminated sexual selection. An independent assay demonstrated that more mature males have higher fitness under polygamy, but this advantage disappears under monogamy. In contrast, for females greater maturity was equally advantageous under polygamy and monogamy. Furthermore, monogamous populations evolved faster development and maturation of females relative to polygamous populations, with no detectable trade-offs with adult size or egg-to-adult survival. These results suggest that a major aspect of male maturation involves developing traits that increase success in sexual competition, whereas female maturation is not limited by investment in traits involved in mate choice or defense against male antagonism. Moreover, rates of juvenile development and adult maturation can readily evolve in opposite directions in the two sexes, possibly implicating polymorphisms with sexually antagonistic pleiotropy.

Sexual selection and assortative mating: an experimental test.

Mate choice and mate competition can both influence the evolution of sexual isolation between populations. Assortative mating may arise if traits and preferences diverge in step, and, alternatively, mate competition may counteract mating preferences and decrease assortative mating. Here, we examine potential assortative mating between populations of Drosophila pseudoobscura that have experimentally evolved under either increased ('polyandry') or decreased ('monogamy') sexual selection intensity for 100 generations. These populations have evolved differences in numerous traits, including a male signal and female preference traits. We use a two males: one female design, allowing both mate choice and competition to influence mating outcomes, to test for assortative mating between our populations. Mating latency shows subtle effects of male and female interactions, with females from the monogamous populations appearing reluctant to mate with males from the polyandrous populations. However, males from the polyandrous populations have a significantly higher probability of mating regardless of the female's population. Our results suggest that if populations differ in the intensity of sexual selection, effects on mate competition may overcome mate choice.

The evolution of sexual imprinting in socially monogamous populations.

Sexual imprinting is a common mechanism of mate preference learning. It is thought to influence how traits evolve and in some cases to promote speciation. Recently there has been increasing interest in how sexual imprinting itself evolves. Theoretical work on polygynous mating systems predicts that females will evolve paternal imprinting, which means they learn to prefer phenotypes expressed by their fathers. In nature however, females of some species learn to prefer phenotypes expressed by their mothers instead. We used a dynamical systems model and tools from adaptive dynamics to study how sexual imprinting evolves in species with socially monogamous mating systems. We considered cases in which the target trait for imprinting is under viability selection but is not a reliable signal of paternal investment. Thus, the target trait signals the genetic benefits rather than the parental care benefits of mate choice. When mating is socially monogamous and there is some extra-pair paternity, we show that maternal imprinting can be favored over paternal imprinting. Counterintuitively, females often become choosier when selecting social partners in systems where extra-pair mating is more frequent. That is, females may be more selective when choosing social partners that will sire a smaller percentage of their offspring. Our results offer new testable hypotheses, and advance our understanding of the mechanisms that drive the evolution of mate choice strategies in nature.

Geographic variation in breeding system and environment predicts melanin-based plumage ornamentation of male and female Kentish plovers.

Sexual selection determines the elaboration of morphological and behavioural traits and thus drives the evolution of phenotypes. Sexual selection on males and females can differ between populations, especially when populations exhibit different breeding systems. A substantial body of literature describes how breeding systems shape ornamentation across species, with a strong emphasis on male ornamentation and female preference. However, whether breeding system predicts ornamentation within species and whether similar mechanisms as in males also shape the phenotype of females remains unclear. Here, we investigate how different breeding systems are associated with male and female ornamentation in five geographically distinct populations of Kentish plovers Charadrius alexandrinus. We predicted that polygamous populations would exhibit more elaborate ornaments and stronger sexual dimorphism than monogamous populations. By estimating the size and intensity of male (n = 162) and female (n = 174) melanin-based plumage ornaments, i.e. breast bands and ear coverts, we show that plumage ornamentation is predicted by breeding system in both sexes. A difference in especially male ornamentation between polygamous (darker and smaller ornaments) and monogamous (lighter and larger) populations causes the greatest sexual dimorphism to be associated with polygamy. The non-social environment, however, may also influence the degree of ornamentation, for instance through availability of food. We found that, in addition to breeding system, a key environmental parameter, rainfall, predicted a seasonal change of ornamentation in a sex-specific manner. Our results emphasise that to understand the phenotype of animals, it is important to consider both natural and sexual selection acting on both males and females.

Evolution of reduced post-copulatory molecular interactions in Drosophila populations lacking sperm competition.

In many species with internal fertilization, molecules transferred in the male ejaculate trigger and interact with physiological changes in females. It is controversial to what extent these interactions between the sexes act synergistically to mediate the female switch to a reproductive state or instead reflect sexual antagonism evolved as a by product of sexual selection on males. To address this question, we eliminated sexual selection by enforcing monogamy in populations of Drosophila melanogaster for 65 generations and then measured the expression of male seminal fluid protein genes and genes involved in the female response to mating. In the absence of sperm competition, male and female reproductive interests are perfectly aligned and any antagonism should be reduced by natural selection. Consistent with this idea, males from monogamous populations showed reduced expression of seminal fluid protein genes, 16% less on average than in polygamous males. Further, we identified 428 genes that responded to mating in females. After mating, females with an evolutionary history of monogamy exhibited lower relative expression of genes that were up regulated in response to mating and higher expression of genes that were down-regulated--in other words, their post-mating transcriptome appeared more virgin-like. Surprisingly, these genes showed a similar pattern even before mating, suggesting that monogamous females evolved to be less poised for mating and the accompanying receipt of male seminal fluid proteins. This reduced investment by both monogamous males and females in molecules involved in post-copulatory interactions points to a pervasive role of sexual conflict in shaping these interactions.

Wealth and the opportunity for sexual selection in men and women

Sexual selection theory suggests that males benefit more than females from multiple mates and that sexual selection is weak in monogamous mating systems. However, little research on sexual selection has been conducted simultaneously in men and women, and we lack a detailed understanding of the socioecological factors that can influence it. Here, we examined the effects of wealth and sex on 2 distinct episodes of human sexual selection (marry once and remarry) in historical Norwegian populations with imposed monogamy, where remarriage was only possible after widowhood. We quantified sexual selection using the Bateman gradient. We also examined the underlying proximate factors that might influence the odds of remarriage and reproduction after widowhood. We found that the intensity of sexual selection corresponds well with Bateman gradients measured in other monogamous populations and was stronger for those who married once than for those who remarried. The selection gradients on “marry once” were affected by neither sex nor wealth. However, when we measured the gradients on “remarry,” sexual selection was stronger on wealthy men and women compared with those who were poor. Remarriage age was the most important underlying factor explaining how widows increased reproductive success. For widowers, it was to remarry a younger woman than themselves. In conclusion, we show that sexual selection can operate on both sexes in a monogamous population and suggest that under certain circumstances (when very wealthy), women can benefit as much as men can by remarriage.

The effects of sexual selection on life‐history traits: an experimental study on guppies

Sexual selection is often prevented during captive breeding in order to maximize effective population size and retain genetic diversity. However, enforcing monogamy and thereby preventing sexual selection may affect population fitness either negatively by preventing the purging of deleterious mutations or positively by reducing sexual conflicts. To better understand the effect of sexual selection on the fitness of small populations, we compared components of female fitness and the expression of male secondary sexual characters in 19 experimental populations of guppies (Poecilia reticulata) maintained under polygamous or monogamous mating regimes over nine generations. In order to generate treatments that solely differed by their level of sexual selection, the middle-class neighbourhood breeding design was enforced in the monogamous populations, while in the polygamous populations, all females contributed similarly to the next generation with one male and one female offspring. This experimental design allowed potential sexual conflicts to increase in the polygamous populations because selection could not operate on adult-female traits. Clutch size and offspring survival showed a weak decline from generation to generation but did not differ among treatments. Offspring size, however, declined across generations, but more in monogamous than polygamous populations. By generation eight, orange- and black-spot areas were larger in males from the polygamous treatment, but these differences were not statistically significant. Overall, these results suggest that neither sexual conflict nor the purging of deleterious mutation had important effects on the fitness of our experimental populations. However, only few generations of enforced monogamy in a benign environment were sufficient to negatively affect offspring size, a trait potentially crucial for survival in the wild. Sexual selection may therefore, under certain circumstances, be beneficial over enforced monogamy during captive breeding.

Male house mice that have evolved with sperm competition have increased mating duration and paternity success

Sperm competition imposes strong selection on males to gain fertilizations and maximize paternity. Males have been shown to adapt to sperm competition by modifying their behaviour and/or reproductive physiology. We investigated the fitness effects of male responses to sperm competition in house mice, Mus domesticus . Males that had been evolving with (polygamy) and without (monogamy) sperm competition for 18 generations were subject to different frequencies of social encounters with conspecific males to generate a sperm competition ‘risk’ treatment and a ‘no risk’ treatment. After manipulation of their social environment for 15–22 days, males were forced to compete for fertilizations against a male with the same selection history that experienced no manipulation. We genotyped embryos at 16 days gestation to quantify paternity success, and thus the competitive ability, of the experimental males. While there was no treatment effect on mating behaviour and paternity success, males from polygamous lines had significantly increased mating duration and paternity success when positioned in the disfavoured role of the second male to mate. Thus, males that had evolved with sperm competition showed greater mating effort and fitness compared to males that had evolved without sperm competition. Whether this is due to a genetic divergence between the lines or a differential capacity of males with different selection histories to respond plastically to current levels of sperm competition remains to be tested. ► Male responses to sperm competition and their fitness effects were studied in mice. ► Different social environments had no effect on mating behaviour and paternity success. ► Males that had evolved via polygamy had increased mating durations and P 2 values. ► Thus, these males had enhanced fitness compared to males from monogamous populations.