RESUMO
Male animals often show higher mutation rates than their female conspecifics. A hypothesis for this male bias is that competition over fertilization of female gametes leads to increased male investment into reproduction at the expense of maintenance and repair, resulting in a trade-off between male success in sperm competition and offspring quality. Here, we provide evidence for this hypothesis by harnessing the power of experimental evolution to study effects of sexual selection on the male germline in the seed beetle Callosobruchus maculatus. We first show that 50 generations of evolution under strong sexual selection, coupled with experimental removal of natural selection, resulted in males that are more successful in sperm competition. We then show that these males produce progeny of lower quality if engaging in sociosexual interactions prior to being challenged to surveil and repair experimentally induced damage in their germline and that the presence of male competitors alone can be enough to elicit this response. We identify 18 candidate genes that showed differential expression in response to the induced germline damage, with several of these previously implicated in processes associated with DNA repair and cellular maintenance. These genes also showed significant expression changes across sociosexual treatments of fathers and predicted the reduction in quality of their offspring, with expression of one gene also being strongly correlated to male sperm competition success. Sex differences in expression of the same 18 genes indicate a substantially higher female investment in germline maintenance. While more work is needed to detail the exact molecular underpinnings of our results, our findings provide rare experimental evidence for a trade-off between male success in sperm competition and germline maintenance. This suggests that sex differences in the relative strengths of sexual and natural selection are causally linked to male mutation bias. The tenet advocated here, that the allocation decisions of an individual can affect plasticity of its germline and the resulting genetic quality of subsequent generations, has several interesting implications for mate choice processes.
Assuntos
Besouros , Sementes , Feminino , Animais , Masculino , Espermatozoides/fisiologia , Células Germinativas , Comportamento Sexual Animal/fisiologia , Besouros/genéticaRESUMO
An often-overlooked aspect of life-history optimization is the allocation of resources to protect the germline and secure safe transmission of genetic information. While failure to do so renders significant fitness consequences in future generations, germline maintenance comes with substantial costs. Thus, germline allocation should trade off with other life-history decisions and be optimized in accordance with an organism's reproductive schedule. Here, we tested this hypothesis by studying germline maintenance in lines of seed beetle, selected for early (E) or late (L) reproduction for 350 and 240 generations, respectively. Female animals provide maintenance and screening of male gametes in their reproductive tract and oocytes. Here, we reveal the ability of young and aged E- and L-females to provide this form of germline maintenance by mating them to males with ejaculates with artificially elevated levels of protein and DNA damage. We find that germline maintenance in E-females peaks at young age and then declines, while the opposite is true for L-females, in accordance with the age of reproduction in the respective regime. These findings identify the central role of allocation to secure germline integrity in life-history evolution and highlight how females can play a crucial role in mitigating the effects of male germline decisions on mutation rate and offspring quality.
Assuntos
Evolução Biológica , Células Germinativas , Longevidade , Animais , Feminino , Masculino , Reprodução , Besouros/fisiologia , Besouros/genéticaRESUMO
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.
Assuntos
Drosophila melanogaster , Comportamento Sexual Animal/fisiologia , Animais , Evolução Biológica , Proteínas de Drosophila/análise , Proteínas de Drosophila/genética , Proteínas de Drosophila/metabolismo , Drosophila melanogaster/genética , Drosophila melanogaster/metabolismo , Drosophila melanogaster/fisiologia , Feminino , Masculino , Proteínas de Plasma Seminal/análise , Proteínas de Plasma Seminal/genética , Proteínas de Plasma Seminal/metabolismo , Transcriptoma/genética , Transcriptoma/fisiologiaRESUMO
Ageing is nearly ubiquitous and encompasses all biological functions. We here focus on age-dependent changes in male reproductive capacity across a broad range of animal taxa. While there has been a long-standing focus on mating ability and overall reproductive success, we here highlight the underlying mechanisms that explain loss in fertilisation capacity in ageing males. Fertilisation is mediated by not only the presence of sperm, but also the cocktail of seminal fluid proteins that ensure sperm survival, capacitation and interaction with female physiology. Sperm ageing has received much attention in studies of male reproductive senescence; however, post-mating processes include a number of interlocked steps that together cumulate in successful fertilisation. As such we consider male ability to elicit female post mating responses such as uterine conformational changes, sperm storage and ovulation and the components within the ejaculate that mediate these post-mating processes. For the latter seminal fluid proteins are key and hence we reflect on age-dependent changes in quality of the entire ejaculate and its consequences for male reproductive capacity. While first studies accrue and highlight that changes in the non-sperm fraction can explain substantial variation in senescent male reproductive success and male ability to induce post-mating responses necessary for fertilisation many open questions still remain that warrant further investigations. One being what the potential age-dependent changes in composition are or whether there is a general decline and how this interacts with sperm to affect fertilisation success. Further, the impact females might have to ameliorate these changes will be an area of interest.
Assuntos
Envelhecimento , Proteínas de Drosophila/metabolismo , Drosophila melanogaster/fisiologia , Ejaculação/fisiologia , Reprodução , Comportamento Sexual Animal/fisiologia , Espermatozoides/fisiologia , Animais , Feminino , Masculino , Sêmen/química , Espermatozoides/citologiaRESUMO
The accessory gland (AG) produces seminal fluid proteins that are transferred to the female upon mating in many insects. These seminal fluid proteins often promote a male's post-copulatory reproductive success. Despite its crucial function many males eclose with a small gland not yet containing the full set of proteins. Thus, they need a physiological maturation period. Using Drosophila melanogaster, we tested whether this physiological maturation is linked to behavioral maturation in males and to what extent seminal fluid allocation patterns are influenced by physiological maturation. To that end, we measured AG protein content (as a proxy for physiological maturation) of young, immature males that were either successful in gaining a mating, but prevented from transferring seminal fluid proteins, or unsuccessful, thus using mating success as a proxy for behavioral maturation. Furthermore, we compared ejaculate allocation in immature and mature males in a single mating. Though mating success and gland maturation increase with male age, we found no evidence for a fine-tuned synchronization of behavioral and physiological maturation in males. This is especially surprising since we found reduced ejaculate allocation in very young, immature males, hinting at reduced fitness benefits from early matings in D. melanogaster.
Assuntos
Proteínas de Drosophila/metabolismo , Drosophila melanogaster/crescimento & desenvolvimento , Drosophila melanogaster/metabolismo , Animais , MasculinoRESUMO
Senescence is accompanied by loss of reproductive functions. Here, we studied reproductive ageing in Drosophila melanogaster males and asked whether the expected decline in male reproductive success is due to diminished functionality of the male accessory gland (AG). The male AG produces the majority of seminal fluid proteins (SFPs) transferred to the female at mating. SFPs induce female postmating changes and are key to male reproductive success. We measured age-dependent gene expression changes for five representative SFP genes in males from four different age groups ranging from 1 to 6 weeks after eclosion. Simultaneously, we also measured male reproductive success in postmating traits mediated by transfer of these five SFPs. We found a decreased in male SFP gene expression with advancing age and an accompanying decline in male postmating success. Hence, male reproductive senescence is associated with a decline in functionality of the male AG. While overall individual SFP genes decreased in expression, our results point towards the idea that the composition of an ejaculate might change with male age as the rate of change was variable for those five genes.
Assuntos
Envelhecimento/genética , Proteínas de Drosophila/genética , Drosophila melanogaster/genética , Animais , Drosophila melanogaster/fisiologia , Feminino , Fertilidade/genética , Expressão Gênica , Masculino , Fenótipo , Sêmen/química , Comportamento Sexual AnimalRESUMO
The ability to learn is key to behavioral adaptation to changing environments. Yet, learning rate and memory retention can vary greatly across or even within species. While interspecific differences have been attributed to ecological context or life history constraints, intraspecific variability in learning behavior is rarely studied and more often, ignored: inferences of the cognitive abilities of a species are most of the time made from experiments using individuals of a single population. Here, we show that learning of host-associated cues in the parasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) shows considerable interpopulation variability, which is at least partly, genetically determined. The strengths of the learning response differed predictably between populations and also varied with the rewarding stimulus. We tested memory retention in a genetically diverse strain and in an iso-female line, bearing a low genetic variability. In addition, we compared our findings with published studies on a third strain using a meta-analytical approach. Our findings suggest that all three strains differ in memory formation from each other. We conclude that, even though the associative learning of host cues is most likely under strong natural selection in parasitoid wasps, considerable genetic variability is maintained at the population as well as at the species level in N. vitripennis.
Assuntos
Vespas/genética , Vespas/fisiologia , Animais , Aprendizagem por Associação , Condicionamento Clássico , Sinais (Psicologia) , Dípteros/parasitologia , Feminino , Variação Genética , Memória , Odorantes , OviposiçãoRESUMO
Climates are changing rapidly, demanding equally rapid adaptation of natural populations. Whether sexual selection can aid such adaptation is under debate; while sexual selection should promote adaptation when individuals with high mating success are also best adapted to their local surroundings, the expression of sexually selected traits can incur costs. Here we asked what the demographic consequences of such costs may be once climates change to become harsher and the strength of natural selection increases. We first adopted a classic life history theory framework, incorporating a trade-off between reproduction and maintenance, and applied it to the male germline to generate formalized predictions for how an evolutionary history of strong postcopulatory sexual selection (sperm competition) may affect male fertility under acute adult heat stress. We then tested these predictions by assessing the thermal sensitivity of fertility (TSF) in replicated lineages of seed beetles maintained for 68 generations under three alternative mating regimes manipulating the opportunity for sexual and natural selection. In line with the theoretical predictions, we find that males evolving under strong sexual selection suffer from increased TSF. Interestingly, females from the regime under strong sexual selection, who experienced relaxed selection on their own reproductive effort, had high fertility in benign settings but suffered increased TSF, like their brothers. This implies that female fertility and TSF evolved through genetic correlation with reproductive traits sexually selected in males. Paternal but not maternal heat stress reduced offspring fertility with no evidence for adaptive transgenerational plasticity among heat-exposed offspring, indicating that the observed effects may compound over generations. Our results suggest that trade-offs between fertility and traits increasing success in postcopulatory sexual selection can be revealed in harsh environments. This can put polyandrous species under immediate risk during extreme heat waves expected under future climate change.
RESUMO
Upon mating, females alter a multitude of physiological and morphological traits to accommodate the demands of reproduction. Changes not only include reproductive tissues but also non-reproductive tissues. For example, in Drosophila melanogaster the gut increases in circumference after mating, likely to facilitate a higher absorption and provision of macronutrients to maturing eggs. A male ejaculatory protein, the sex peptide, is instrumental to mediating several post-mating changes and receipt increases nutrient uptake as well as shifts taste preferences in mated females. We here tested whether sex peptide receipt also alters the protein: carbohydrate ratio at which females maximize their fitness. To test this, we mated females to males lacking sex peptide or control males and fed them with known volumes and concentrations of sugar and yeast. This enabled us to determine how the sugar to yeast ratio affects lifetime egg output as well as lifespan of females mated to the two male types. Sex peptide did not shift the optimal ratio. Instead, sex peptide receipt aided females in increasing their egg output at low macronutrient concentrations, but this advantage disappeared at higher macronutrient intake rates. Assuming that nutrient limitation might be common, then receipt of SP is beneficial under poor conditions.
Assuntos
Proteínas de Drosophila , Drosophila melanogaster , Animais , Proteínas de Drosophila/metabolismo , Drosophila melanogaster/fisiologia , Feminino , Masculino , Nutrientes , Óvulo/metabolismo , Peptídeos/metabolismo , Reprodução/fisiologia , Saccharomyces cerevisiae , Comportamento Sexual Animal/fisiologia , Açúcares/metabolismoRESUMO
In variable environments, sampling information on habitat quality is essential for making adaptive foraging decisions. In insect parasitoids, females foraging for hosts have repeatedly been shown to employ behavioral strategies that are in line with predictions from optimal foraging models. Yet, which cues exactly are employed to sample information on habitat quality has rarely been investigated. Using the gregarious parasitoid Nasonia vitripennis (Walker; Hymenoptera: Pteromalidae), we provided females with different cues about hosts to elucidate, which of them would change a wasp's posterior behavior suggesting a change in information status. We employed posterior clutch size decisions on a host as proxy for a female's estimation of habitat quality. Taking into account changes in physiological state of the foraging parasitoid, we tested whether different host qualities encountered previously change the subsequent clutch size decision in females. Additionally, we investigated whether other kinds of positive experiences-such as ample time to investigate hosts, host feeding, or egg laying-would increase a wasp's estimated value of habitat quality. Contrary to our expectations, quality differences in previously encountered hosts did not affect clutch size decisions. However, we found that prior egg laying experience changes posterior egg allocation to a host, indicating a change in female information status. Host feeding and the time available for host inspection, though correlated with egg laying experience, did not seem to contribute to this change in information status.
RESUMO
Mating bears costs, but how these costs affect the senescence of reproductive traits in males has received relatively little attention. Males of many species show reduced benefits from pre- and post-copulatory reproductive traits during ageing. Senescence of post-copulatory reproductive traits is often linked to a reduction in sperm quantity and quality, but can also be a consequence of changes in seminal fluid proteins that are transferred alongside sperm during mating. Here we investigated how mating history affects male reproductive ageing, especially at the post-copulatory level, using Drosophila melanogaster, a species in which links between seminal fluid proteins and male reproductive traits are well established. Besides a male cohort kept virgin until the start of the experiment we also included a cohort of males kept together with females allowing for ample mating opportunities. With these males we conducted a series of behavioral experiments covering several aspects of male reproductive success with males ranging in age from 4â¯days to 6â¯weeks after eclosion. Additionally, we investigated the storage capacity of male accessory glands (AG), the production site of the majority of seminal fluid proteins. We found male reproductive success to decline with increasing male age and, most importantly, males with prior matings showed a reduced performance in pre-copulatory success. However, our data suggest a constant short-term cost of mating rather than an accelerated senescence of pre-copulatory traits. In contrast, senescence of post-copulatory reproductive traits differed between mated and virgin males, hinting at mating costs in males altering the ageing process. We could not find any differences in the capacity of the AG to store seminal fluid proteins, however, our data suggest that old males transfer fewer seminal fluid proteins in a single mating. We conclude that a variety of traits is affected by male reproductive ageing in D. melanogaster with the cost of mating varying in its impact on senescence in these traits.
Assuntos
Envelhecimento , Drosophila melanogaster/fisiologia , Fenótipo , Comportamento Sexual Animal , Animais , Proteínas de Drosophila/metabolismo , Proteínas de Insetos/metabolismo , Longevidade , Masculino , ReproduçãoRESUMO
Male reproductive ageing has been mainly explained by a reduction in sperm quality with negative effects on offspring development and quality. In addition to sperm, males transfer seminal fluid proteins (Sfps) at mating; Sfps are important determinants of male reproductive success. Receipt of Sfps leads to female post-mating changes including physiological changes, and affects sperm competition dynamics. Using the fruit fly Drosophila melanogaster we studied ageing males' ability to induce female post-mating responses and determined the consequences of male ageing on their reproductive success. We aged males for up to 7weeks and assayed their ability to: i) gain a mating, ii) induce egg-laying and produce offspring, iii) prevent females from remating and iv) transfer sperm and elicit storage after a single mating. We found that with increasing age, males were less able to induce post-mating responses in their mates; moreover ageing had negative consequences for male success in competitive situations. Our findings indicate that with advancing age male flies transferred less effective ejaculates and that Sfp composition might change over a male's lifetime in quantity and/or quality, significantly affecting his reproductive success.
Assuntos
Envelhecimento/fisiologia , Drosophila melanogaster/fisiologia , Fertilidade/fisiologia , Espermatozoides/fisiologia , Animais , Proteínas de Drosophila/fisiologia , Feminino , Masculino , Oviposição , Contagem de EspermatozoidesRESUMO
Competition between males creates potential for pre- and postcopulatory sexual selection and conflict. Theory predicts that males facing risk of sperm competition should evolve traits to secure their reproductive success. If those traits are costly to females, the evolution of such traits may also increase conflict between the sexes. Conversely, under the absence of sperm competition, one expectation is for selection on male competitive traits to relax thereby also relaxing sexual conflict. Experimental evolution studies are a powerful tool to test this expectation. Studies in multiple insect species have yielded mixed and partially conflicting results. In this study, we evaluated male competitive traits and male effects on female costs of mating in Drosophila melanogaster after replicate lines evolved for more than 50 generations either under enforced monogamy or sustained polygamy, thus manipulating the extent of intrasexual competition between males. We found that in a setting where males competed directly with a rival male for access to a female and fertilization of her ova polygamous males had superior reproductive success compared to monogamous males. When comparing reproductive success solely in double mating standard sperm competition assays, however, we found no difference in male sperm defense competitiveness between the different selection regimes. Instead, we found monogamous males to be inferior in precopulatory competition, which indicates that in our system, enforced monogamy relaxed selection on traits important in precopulatory rather than postcopulatory competition. We discuss our findings in the context of findings from previous experimental evolution studies in Drosophila ssp. and other invertebrate species.