SEXUAL SELECTION AFFECTS THE EVOLUTION OF LIFESPAN AND AGEING IN THE DECORATED CRICKET GRYLLODES SIGILLATUS

Recent work suggests that sexual selection can influence the evolution of ageing and lifespan by shaping the optimal timing and relative costliness of reproductive effort in the sexes. We used inbred lines of the decorated cricket, Gryllodes sigillatus, to estimate the genetic (co)variance between age‐dependent reproductive effort, lifespan, and ageing within and between the sexes. Sexual selection theory predicts that males should die sooner and age more rapidly than females. However, a reversal of this pattern may be favored if reproductive effort increases with age in males but not in females. We found that male calling effort increased with age, whereas female fecundity decreased, and that males lived longer and aged more slowly than females. These divergent life‐history strategies were underpinned by a positive genetic correlation between early‐life reproductive effort and ageing rate in both sexes, although this relationship was stronger in females. Despite these sex differences in life‐history schedules, age‐dependent reproductive effort, lifespan, and ageing exhibited strong positive intersexual genetic correlations. This should, in theory, constrain the independent evolution of these traits in the sexes and may promote intralocus sexual conflict. Our study highlights the importance of sexual selection to the evolution of sex differences in ageing and lifespan in G. sigillatus.     

Reproductive ageing and sexual selection on male body size in a wild population of antler flies (Protopiophila litigata)

Little is known about the importance of trade-offs between ageing and other life history traits, or the effects of ageing on sexual selection, particularly in wild populations suffering high extrinsic mortality rates. Life history theory suggests that trade-offs between reproduction and somatic maintenance may constrain individuals with higher initial reproductive rates to deteriorate more rapidly, resulting in reduced sexual selection strength. However, this trade-off may be masked by increased condition dependence of reproductive effort in older individuals. We tested for this trade-off in males in a wild population of antler flies (Protopiophila litigata). High mating rate was associated with reduced longevity, as a result of increased short-term mortality risk or accelerated ageing in traits affecting viability. In contrast, large body size was associated with accelerated ageing in traits affecting mating success, resulting in reduced sexual selection for large body size. Thus, ageing can affect sexual selection and evolution in wild populations.     

Sexual selection and conflict as engines of ecological diversification

Ecological diversification presents an enduring puzzle: how do novel ecological strategies evolve in organisms that are already adapted to their ecological niche? Most attempts to answer this question posit a primary role for genetic drift, which could carry populations through or around fitness "valleys" representing maladaptive intermediate phenotypes between alternative niches. Sexual selection and conflict are thought to play an ancillary role by initiating reproductive isolation and thereby facilitating divergence in ecological traits through genetic drift or local adaptation. Here, I synthesize theory and evidence suggesting that sexual selection and conflict could play a more central role in the evolution and diversification of ecological strategies through the co-optation of sexual traits for viability-related functions. This hypothesis rests on three main premises, all of which are supported by theory and consistent with the available evidence. First, sexual selection and conflict often act at cross-purposes to viability selection, thereby displacing populations from the local viability optimum. Second, sexual traits can serve as preadaptations for novel viability-related functions. Third, ancestrally sex-limited sexual traits can be transferred between sexes. Consequently, by allowing populations to explore a broad phenotypic space around the current viability optimum, sexual selection and conflict could act as powerful drivers of ecological adaptation and diversification.     

Ancestral populations perform better in a novel environment: domestication of medfly populations from five global regions

Geographically isolated populations of a species may differ in several aspects of life-history, morphology, behavior, and genetic structure as a result of adaptation in ecologically diverse habitats. We used a global invasive species, the Mediterranean fruit fly to investigate, whether adaptation to a novel environment differs among geographically isolated populations that vary in major life history components such as life span and reproduction. We used wild populations from five global regions (Kenya, Hawaii, Guatemala, Portugal, and Greece). Adult demographic traits were monitored in F(2), F(5), F(7) and F(9) generations in captivity. Although domestication in constant laboratory conditions had a different effect on the mortality and reproductive rates of the different populations, a general trend of decreasing life span and age of first reproduction was observed for most medfly populations tested. However, taking into account longevity of both sexes, age-specific reproductive schedules, and average reproductive rates we found that the ancestral Kenyan population kept the above life history traits stable during domestication compared to the other populations tested. These findings provide important insights in the life-history evolution of this model species, and suggest that ancestral medfly populations perform better than the derived - invasive ones in a novel environment.     

THE ROLES OF LIFE‐HISTORY SELECTION AND SEXUAL SELECTION IN THE ADAPTIVE EVOLUTION OF MATING BEHAVIOR IN A BEETLE

Although there is continuing debate about whether sexual selection promotes or impedes adaptation to novel environments, the role of mating behavior in such adaptation remains largely unexplored. We investigated the evolution of mating behavior (latency to mating, mating probability and duration) in replicate populations of seed beetles Callosobruchus maculatus subjected to selection on life‐history (“Young” vs. “Old” reproduction) under contrasting regimes of sexual selection (“Monogamy” vs. “Polygamy”). Life‐history selection is predicted to favor delayed mating in “Old” females, but sexual conflict under polygamy can potentially retard adaptive life‐history evolution. We found that life‐history selection yielded the predicted changes in mating behavior, but sexual selection regime had no net effect. In within‐line crosses, populations selected for late reproduction showed equally reduced early‐life mating probability regardless of mating system. In between‐line crosses, however, the effect of life‐history selection on early‐life mating probability was stronger in polygamous lines than in monogamous ones. Thus, although mating system influenced male–female coevolution, removal of sexual selection did not affect the adaptive evolution of mating behavior. Importantly, our study shows that the interaction between sexual selection and life‐history selection can result in either increased or decreased reproductive divergence depending on the ecological context.     

Sexual Conflict,Life Span,and Aging

The potential for sexual conflict to influence the evolution of life span and aging has been recognized for more than a decade, and recent work also suggests that variation in life span and aging can influence sexually antagonistic coevolution. However, empirical exploration of these ideas is only beginning. Here, we provide an overview of the ideas and evidence linking inter- and intralocus sexual conflicts with life span and aging. We aim to clarify the conceptual basis of this research program, examine the current state of knowledge, and suggest key questions for further investigation.Sexual conflict arises because the sexes maximize their fitness via different, and often mutually incompatible, strategies, and its signature has been detected across a wide range of morphological, physiological, behavioral, and life-history traits in many species. A number of investigators have suggested that sexual conflict could play an important role in the evolution of two particularly interesting life-history traits: life span and aging (Svensson and Sheldon 1998; Promislow 2003; Bonduriansky et al. 2008; Maklakov and Lummaa 2013). Sexual conflict can affect life span and aging rate at both proximate (within-generation) and ultimate (evolutionary) scales. Sexually antagonistic behavioral or physiological interactions that increase mortality rate in one or both sexes (interlocus sexual conflict) could drive the evolution of faster life histories. Moreover, sex-specific optimization of reproductive strategies may often result in sex differences in life span and aging rates, and sexually antagonistic selection on shared genetic architecture can displace one or both sexes from their sex-specific optima for these traits (intralocus sexual conflict). Conversely, a change in life histories because of environmental fluctuations could affect the degree of sexual conflict in a population and influence sexual coevolution. Although evidence for sexual conflict is rapidly accumulating, our understanding of its relationship to life span and aging remains rudimentary. In this review, we provide a critical review of recent literature and highlight areas that require further investigation.     

Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle

Males and females have different routes to successful reproduction, resulting in sex differences in lifespan and age-specific allocation of reproductive effort. The trade-off between current and future reproduction is often resolved differently by males and females, and both sexes can be constrained in their ability to reach their sex-specific optima owing to intralocus sexual conflict. Such genetic antagonism may have profound implications for evolution, but its role in ageing and lifespan remains unresolved. We provide direct experimental evidence that males live longer and females live shorter than necessary to maximize their relative fitness in Callosobruchus maculatus seed beetles. Using artificial selection in a genetically heterogeneous population, we created replicate long-life lines where males lived on average 27 per cent longer than in short-life lines. As predicted by theory, subsequent assays revealed that upward selection on male lifespan decreased relative male fitness but increased relative female fitness compared with downward selection. Thus, we demonstrate that lifespan-extending genes can help one sex while harming the other. Our results show that sexual antagonism constrains adaptive life-history evolution, support a novel way of maintaining genetic variation for lifespan and argue for better integration of sex effects into applied research programmes aimed at lifespan extension.     

Rapid adaptation to a novel host in a seed beetle (Callosobruchus maculatus): the role of sexual selection

Rapid diversification is common among herbivorous insects and is often the result of host shifts, leading to the exploitation of novel food sources. This, in turn, is associated with adaptive evolution of female oviposition behavior and larval feeding biology. Although natural selection is the typical driver of such adaptation, the role of sexual selection is less clear. In theory, sexual selection can either accelerate or impede adaptation. To assess the independent effects of natural and sexual selection on the rate of adaptation, we performed a laboratory natural selection experiment in a herbivorous bruchid beetle (Callosobruchus maculatus). We established replicated selection lines where we varied natural (food type) and sexual (mating system) selection in a 2 x 2 orthogonal design, and propagated our lines for 35 generations. In half of the lines, we induced a host shift whereas the other half was kept on the ancestral host. We experimentally enforced monogamy in half of the lines, whereas the other half remained polygamous. The beetles rapidly adapted to the novel host, which primarily involved increased host acceptance by females and an accelerated rate of larval development. We also found that our mating system treatment affected the rate of adaptation, but that this effect was contingent upon food type. As beetles adapted to the novel host, sexual selection reinforced natural selection whereas populations residing close to their adaptive peak (i.e., those using their ancestral host) exhibited higher fitness in the absence of sexual selection. We discuss our findings in light of current sexual selection theory and suggest that the net evolutionary effect of reproductive competition may critically depend on natural selection. Sexual selection may commonly accelerate adaptation under directional natural selection whereas sexual selection, and the associated load brought by sexual conflict, may tend to depress population fitness under stabilizing natural selection.     

Sexual Conflict over the Maintenance of Sex: Effects of Sexually Antagonistic Coevolution for Reproductive Isolation of Parthenogenesis

Sexual reproduction involves many costs. Therefore, females acquiring a capacity for parthenogenetic (or asexual) reproduction will gain a reproductive advantage over obligately sexual females. In contrast, for males, any trait coercing parthenogens into sexual reproduction (male coercion) increases their fitness and should be under positive selection because parthenogenesis deprives them of their genetic contribution to future generations. Surprisingly, although such sexual conflict is a possible outcome whenever reproductive isolation is incomplete between parthenogens and the sexual ancestors, it has not been given much attention in the studies of the maintenance of sex. Using two mathematical models, I show here that the evolution of male coercion substantially favours the maintenance of sex even though a female barrier against the coercion can evolve. First, the model based on adaptive-dynamics theory demonstrates that the resultant antagonistic coevolution between male coercion and a female barrier fundamentally ends in either the prevalence of sex or the co-occurrence of two reproductive modes. This is because the coevolution between the two traits additionally involves sex-ratio selection, that is, an increase in parthenogenetic reproduction leads to a female-biased population sex ratio, which will enhance reproductive success of more coercive males and directly promotes the evolution of the coercion among males. Therefore, as shown by the individual-based model, the establishment of obligate parthenogenesis in the population requires the simultaneous evolution of strong reproductive isolation between males and parthenogens. These findings should shed light on the interspecific diversity of reproductive modes as well as help to explain the prevalence of sexual reproduction.     

Sex differences in nutrient-dependent reproductive ageing

Evolutionary theories of aging predict that fitness-related traits, including reproductive performance, will senesce because the strength of selection declines with age. Sexual selection theory predicts, however, that male reproductive performance (especially sexual advertisement) will increase with age. In both bodies of theory, diet should mediate age-dependent changes in reproductive performance. In this study, we show that the sexes exhibit dramatic, qualitative differences in age-dependent reproductive performance trajectories and patterns of reproductive ageing in the cricket Teleogryllus commodus. In females, fecundity peaked early in adulthood and then declined. In contrast, male sexual advertisement increased across the natural lifespan and only declined well beyond the maximum field lifespan. These sex differences were robust to deviations from sex-specific dietary requirements. Our results demonstrate that sexual selection can be at least as important as sex-dependent mortality in shaping the signal of reproductive ageing.     

Cost-free lifespan extension via optimization of gene expression in adulthood aligns with the developmental theory of ageing

Ageing evolves because the force of selection on traits declines with age but the proximate causes of ageing are incompletely understood. The ‘disposable soma’ theory of ageing (DST) upholds that competitive resource allocation between reproduction and somatic maintenance underpins the evolution of ageing and lifespan. In contrast, the developmental theory of ageing (DTA) suggests that organismal senescence is caused by suboptimal gene expression in adulthood. While the DST predicts the trade-off between reproduction and lifespan, the DTA predicts that age-specific optimization of gene expression can increase lifespan without reproduction costs. Here we investigated the consequences for lifespan, reproduction, egg size and individual fitness of early-life, adulthood and post-reproductive onset of RNAi knockdown of five ‘longevity’ genes involved in key biological processes in Caenorhabditis elegans. Downregulation of these genes in adulthood and/or during post-reproductive period increases lifespan, while we found limited evidence for a link between impaired reproduction and extended lifespan. Our findings demonstrate that suboptimal gene expression in adulthood often contributes to reduced lifespan directly rather than through competitive resource allocation between reproduction and somatic maintenance. Therefore, age-specific optimization of gene expression in evolutionarily conserved signalling pathways that regulate organismal life histories can increase lifespan without fitness costs.     

Asexual and sexual reproductive strategies in clonal plants

Most plants can reproduce both sexually and asexually (or vegetatively),and the balance between the two reproductive modes may vary widely between and within species.Extensive clonal growth may affect the evolution of life history traits in many ways.First,in some clonal species,sexual reproduction and sex ratio vary largely among populations.Variation in sexual reproduction may strongly affect plant's adaptation to local environments and the evolution of the geographic range.Second,clonal growth can increase floral display,and thus pollinator attraction,while it may impose serious constraints and evolutionary challenges on plants through geitonogamy that may strongly influence pollen dispersal.Geitonogamous pollination can bring a cost to plant fitness through both female and male functions.Some co-evolutionary interactions,therefore,may exist between the spatial structure and the mating behavior of clonal plants.Finally,a trade-off may exist between sexual reproduction and clonal growth.Resource allocation to the two reproductive modes may depend on environmental conditions,competitive dominance,life span,and genetic factors.If different reproductive modes represent adaptive strategies for plants in different environments,we expect that most of the resources should be allocated to sexual reproduction in habitats with fluctuating environmental conditions and strong competition,while clonal growth should be dominant in stable habitats.Yet we know little about the consequence of natural selection on the two reproductive modes and factors which control the balance of the two reproductive modes.Future studies should investigate the reproductive strategies of clonal plants simultaneously from both sexual and asexual perspectives.     

克隆植物的无性与有性繁殖对策

许多植物同时具有克隆生长与有性繁殖,两种繁殖方式间的平衡在不同物种间以及同一物种内不同种群间变化很大。旺盛的克隆生长可能会从多方面影响生活史进化。首先,许多克隆植物的有性繁殖与更新程度都很低,甚至有一些植物由于克隆生长而几乎完全放弃了有性过程,从而影响到克隆植物对局域环境的适应和地理范围进化。其次,克隆生长增大花展示进而增加了对传粉者的吸引,同时也增加了同株异花授粉的风险,而同株异花授粉往往会导致植物雄性和雌性适合度的下降。因此,克隆植物的空间结构与交配方式间可能存在着协同进化关系。最后,克隆生长与有性繁殖间可能存在着权衡关系:对克隆生长的资源投入将会减少对有性繁殖的资源投入。这种权衡关系可能是由环境条件、竞争力度、植物寿命和遗传等因素决定的。如果不同的繁殖方式是植物在不同环境下采取的适应性对策,那么我们可以预期:在波动和竞争力度大的生境中,植物应将大部分的繁殖资源分配给有性繁殖;而在相对稳定的环境中,克隆繁殖应该占据优势地位。但是自然选择对两种繁殖方式的选择结果是什么,以及控制这两种方式间平衡的生态和遗传因子究竟有哪些,到底是克隆生长单向地影响了植物的有性繁殖,还是与有性过程相伴随的选择压力同时塑造了植物的克隆习性?目前尚不清楚。同时从无性与有性繁殖两个方面综合考察克隆植物的繁殖对策是今后亟待加强的工作。     

性选择与性冲突理论在植物繁殖生态学中的应用与进展

性选择与性冲突是植物繁殖性状多样性及性系统演化的重要动力, 二者密切相关却又有所区别, 理解它们的作用机制及其影响对于植物繁殖生态学的研究具有重要意义。当前, 性选择与性冲突理论在植物繁殖生态学中的运用已取得长足进展, 但国内相关研究较少, 对该领域关注不够。因此, 该文对该领域的基本理论和研究进展进行了综述。首先, 阐述性选择与性冲突理论在植物研究中的发展及其运用基础; 其次, 分别从授粉前和授粉后两个阶段详细介绍性选择与性冲突在有花植物繁殖过程中的作用机制及其影响, 并指出环境因素对它们所产生的影响; 最后, 对当前研究存在的不足及该领域未来的研究方向进行总结和展望。希望以此增强人们对性选择和性冲突理论的认识, 促进其在植物繁殖生态学中的运用与发展。     

Sexual selection and senescence: do seed beetle males (Acanthoscelides obtectus,Bruchidae, Coleoptera) shape the longevity of their mates?

Although the reasons why organisms age and die are generally well understood, it has recently been suggested that an optimal life span has evolved not only as the result of trade‐offs between reproductive performances early and late in life, but also that a balance between the costs and benefits of the number of mating has also played an important role in the evolution of ageing in both sexes. By using four seed beetle (Acanthoscelides obtectus) lines selected for different life history traits, but which have also inadvertently created monoandrous and polyandrous conditions, we showed that males evolved to affect the mortality patterns of females in a way consistent to the postmating sexual selection generated by sexually antagonistic co‐evolution theory. Monoandrous males, irrespectively of body weight and other life history traits specific to their lines, evolved to increase the longevity of control females kept under starvation and suppressed fecundity, compared with males that originated in the lines with effectively polyandrous conditions. When females were allowed to lay eggs, the effects of males from different lines and mating type history on the senescence of females were substantially weaker. We found that males in the line that was evolved to decelerate senescence and polyandrous conditions stimulate the earlier onset of females’ oviposition, relative to males stemmed from the line with accelerated senescence and monoandrous conditions. This fact may explain the absence of difference in the mean longevities between the control females mated to these males and highlight the importance of sexual selection in the evolution of ageing.     

Sexual reproduction and diversity: Connection between sexual selection and biological communities via population dynamics

Sexual reproduction is a mysterious phenomenon. Most animals and plants invest in sexual reproduction, even though it is more costly than asexual reproduction. Theoretical studies suggest that occasional or conditional use of sexual reproduction, involving facultative switching between sexual and asexual reproduction, is the optimal reproductive strategy. However, obligate sexual reproduction is common in nature. Recent studies suggest that the evolution of facultative sexual reproduction is prevented by males that coerce females into sexual fertilization; thus, sexual reproduction has the potential to enforce costs on a given species. Here, the effect of sex on biodiversity is explored by evaluating the reproductive costs arising from sex. Sex provides atypical selection pressure that favors traits that increase fertilization success, even at the expense of population growth rates, that is, sexual selection. The strength of sexual selection depends on the density of a given species. Sexual selection often causes strong negative effects on the population growth rates of species that occur at high density. Conversely, a species that reduces its density is released from this negative effect, and so increases its growth rate. Thus, this negative density-dependent effect on population growth that arises from sexual selection could be used to rescue endangered species from extinction, prevent the overgrowth of common species and promote the coexistence of competitive species. Recent publications on sexual reproduction provide several predictions related to the evolution of reproductive strategies, which is an important step toward integrating evolutionary dynamics, demographic dynamics and community dynamics.     

Genetic correlations with floral display lead to sexual dimorphism in the cost of reproduction

In dioecious plants, females typically invest more biomass in reproduction than males and consequently experience stronger life-history trade-offs. Sexual dimorphism in life history runs counter to this pattern in Silene latifolia: females acquire less carbon and invest more biomass in reproduction, but males pay a higher cost of reproduction. The species is sexually dimorphic for many traits, especially flower number, with males producing many, small flowers compared to females. We tested whether the cost of reproduction is higher in males because flower number, which we presume to be under sexual selection in males, is genetically correlated with traits that would affect life-history trade-offs. We performed artificial selection to reduce the sexual dimorphism in flower size and looked at correlated responses in ecophysiological traits. We found significant correlated responses in total vegetative mass, leaf mass, leaf thickness, and measures of CO(2) exchange. Individuals in the many-and-small-flowered selection lines did not grow as large or invest as much biomass in leaves, and their leaves exhibited an up-regulated physiology that shortened leaf life span. Our results are consistent with the hypothesis that genetic correlations between floral display and ecophysiological traits lead to a higher cost of reproduction for males.     

Natural selection and divergence in mate preference during speciation

Sexual isolation can evolve due to natural selection against hybrids (reinforcement). However, many different forms of hybrid dysfunction, and selective processes that do not involve hybrids, can contribute to the evolution of sexual isolation. Here we review how different selective processes affect the evolution of sexual isolation, describe approaches for distinguishing among them, and assess how they contribute to variation in sexual isolation among populations of Timema cristinae stick-insects. Pairs of allopatric populations of T. cristinae living on different host-plant species exhibit greater sexual isolation than those on the same host, indicating that some sexual isolation has evolved due to host adaptation. Sexual isolation is strongest in regions where populations on different hosts are in geographic contact, a pattern of reproductive character displacement that is indicative of reinforcement. Ecological costs to hybridization do occur but traits under ecological selection (predation) do not co-vary strongly with the probability of between-population mating such that selection on ecological traits is not predicted to produce a strong correlated evolutionary response in mate preference. Moreover, F1 hybrid egg inviability is lacking and the factors contributing to reproductive character displacement require further study. Finally, we show that sexual isolation involves, at least in part, olfactory communication. Our results illustrate how understanding of the evolution of sexual isolation can be enhanced by isolating the roles of diverse ecological and evolutionary processes.     

Sexual selection: an evolutionary force in plants?

Sexual selection has traditionally been used to explain exaggerated sexual traits in male animals. Today the concept has been developed and various other sexually related traits have been suggested to evolve in the same manner. In nearly all new areas where the theory of sexual selection has been applied, there has been an intense debate as to whether the application is justified. Is it the case that some scientists are all too ready to employ fashionable ideas? Or are there too many dogmatic researchers refusing to accept that science develops and old ideas are transformed? Maybe the controversies are simply a reflection of the difficulty of defining a theory under constant re‐evaluation. Thus, we begin by summarizing the theory of sexual selection in order to assess the influence of sexual selection on the evolution of plant morphology. We discuss empirical findings concerning potentially affected traits. Although we have tried to address criticisms fairly, we still conclude that sexual selection can be a useful tool when studying the evolution of reproductive traits in plants. Furthermore, by including the evidence from an additional kingdom, a fuller understanding of the processes involved in sexual selection can be gained.     

Evolutionary links between reproductive morphology, ecology and mating behavior in opisthobranch gastropods

Sexual coevolution in morphological and behavioral traits has rarely been studied. Using phylogenetic analyses, we explore relationships between sexual characters based on a new molecular phylogeny of 33 opisthobranch taxa (Aglajidae and Gastropteridae). Our measurements of these simultaneous hermaphrodites include male and female reproductive anatomy, mating behavior, and spatial gregariousness. After phylogenetic correction, we found evidence for correlated evolution between male and female reproductive organs such as the size of the seminal fluid producing prostate gland and that of the sperm digesting bursa copulatrix. Our findings suggest that reproductive trait variation is mediated by sexual coevolution, where putatively manipulative male organs evolved in association with female organs involved in sperm selection. Furthermore, low gregariousness was associated with long, reciprocal copulations. We interpret this result as an adaptation to infrequent mate encounters, where it pays to mate longer with and presumably transfer more sperm to a rare partner. Several complex reproductive traits were repeatedly gained or lost across our phylogeny. This pattern is consistent with a scenario in which sexual selection generates dynamic coevolutionary cycles similar to those expected under sexual antagonism. We finally outline approaches for experimentally assessing the proposed functional links that underlie the evolutionary correlations revealed by our study.