Males must partition their limited reproductive investments between traits that promote access to females (sexual ornaments and weapons) and traits that enhance fertilization success, such as testes and ejaculates. Recent studies show that if the most weaponized males can monopolize access to females through contest competition, thereby reducing the risk of sperm competition, they tend to invest less in sperm production. However, how males invest in sexual ornaments relative to sperm production remains less clear. If male ornaments serve as badges of status, with high-ranking males attaining near-exclusive access to females, similar to monopolizing females through combat, their expression should also covary negatively with investment in post-mating traits. In a comparative study across primates, which exhibit con- siderable diversification in sexual ornamentation, male weaponry and testes size, we found relative testes size to decrease with sexual ornaments but increase with canine size. These contrasting evolutionary trajectories might be driven by differential selection, functional constraints or temporal patterns of metabolic investment between the different types of sexual traits. Impor- tantly, however, our results indicate that the theory of relative investments between weapons and testes in the context of monopolizing females can extend to male ornaments.
Full text: doi:10.1098/rspb.2018.2542
Sperm morphological variation has attracted considerable interest and generated a wealth of (mostly descriptive) studies over the past three centuries. Yet, apart from biophysical studies linking sperm morphology to swimming velocity, surprisingly little is known about the adaptive significance of sperm form and the selective processes underlying its tremendous diversification throughout the animal kingdom. Here, we first discuss the challenges of examining sperm morphology in an evolutionary context and why our understanding of it is still so poor. Then, we review empirical evidence for how sexual selection theory applies to the evolution of sperm form and function, including putative secondary sexual traits borne by sperm.
Full text: doi:10.1530/REP-17-0536
Support for macroecological rules in insects is mixed, with potential confounding interrelations between patterns rarely studied. We here investigate global patterns in body and wing size, sexual size dimorphism and range size in common fruit flies (Diptera: Drosophilidae) and explore potential interrelations and the predictive power of Allen's, Bergmann's, Rensch's and Rapoport's rules. We found that thorax length (r2 = 0.05) and wing size (r2 = 0.09) increased with latitude, supporting Bergmann's rule. Contrary to patterns often found in endothermic vertebrates, relative wing size increased towards the poles (r2 = 0.12), a pattern against Allen's rule, which we attribute to selection for increased flight capacity in the cold. Sexual size dimorphism decreased with size, evincing Rensch's rule across the family (r2 = 0.14). Yet, this pattern was largely driven by the virilis – repleta radiation and only weakly in other lineages. Finally, range size did not correlate with latitude, although a positive relationship with latitude was present in a subset of the species investigated, providing no convincing evidence for Rapoport's rule. We further found little support for confounding interrelations between body size, wing loading and range size in this taxon. Nevertheless, we demonstrate that studying several traits simultaneously at minimum permits better interpretation in case of multiple, potentially conflicting trends or hypotheses concerning the macroecology of insects.
Full text: doi:10.1111/ecog.03382
Sexual size dimorphism (SSD), caused by sexually antagonistic selection, can vary drastically across environments, demonstrating pronounced sex-specific plasticity. In insects, females are usually the larger and more plastic sex. However, the shortage of taxa with male-biased SSD hampers the assessment of whether the greater plasticity in females is driven by selection on size or represents an effect of the female reproductive role. Here we specifically address the role of sex-specific plasticity, or condition dependence, of body size in the evolution of SSD reversals to disentangle sex and size effects. We first investigate sex-specific body size plasticity in Sepsis punctum and S. neocynipsea as two independent cases of intraspecific SSD reversals in sepsid flies. In both species, directional variation in SSD between populations is driven by stronger sexual selection on male size. Using controlled laboratory breeding, we find evidence for sex-specific plasticity and increased condition dependence of male size in populations with male-biased SSD, but not of female size in populations with female-biased SSD, indicating no adaptive canalization of female size. To extend the comparative scope, we next estimate sex-specific body size plasticity in eight additional fly species that differ in the direction of SSD under laboratory conditions. In all species with male-biased SSD we find males to be the more plastic sex, while this was only rarely the case in species with female-biased SSD, thus suggesting a more general trend in Diptera. To examine the generality of this pattern in holometabolous insects, we combine our data with data from the literature in a meta-analysis. Again, male body size tends to be more plastic than female size when males are the larger sex, though female size is now also generally more plastic when females are larger. Our findings indicate that primarily selection on size, rather than the reproductive role per se, drives the evolution of sex-specific body size plasticity. However, sepsid flies, and possibly Diptera in general, show a clear sexual asymmetry with greater male than female plasticity related to SSD, likely driven by strong sexual selection on males. Although further research controlling for phylogenetic and ecological confounding effects is needed, our findings are congruent with theory in suggesting that condition dependence plays a pivotal role in the evolution of sexual size dimorphism.
Full text: doi:10.1111/1365-2435.13004
The evolution of sperm quality and quantity is shaped by various selective processes, with sperm competition generally considered the primary selective agent. Particularly in external fertilizers, however, sperm limitation through gamete dispersal can also influence gamete investments, but empirical data examining this effect are limited. Here, we studied the relative importance of sperm competition and the spawning conditions in explaining the macroevolutionary patterns of sperm size and number within two taxa with external fertilization but differences in their reproductive biology. In frogs, sperm swim slowly but for up to hours as they penetrate the gelatinous egg coating, whereas fish sperm typically swim fast, are very short-lived (seconds to minutes), and often face a relatively higher risk of being moved away from the ova by currents. Our phylogenetic models and path analyses revealed different trajectories of ejaculate evolution in these two taxa. Sperm size and number responded primarily to variation in sperm competition in the anurans, but more strongly to egg number and water turbulence in the fishes. Whereas the results across anurans align with the general expectation that sexual selection is the main driver of ejaculate evolution, our findings across the fishes suggest that sperm limitation has been underappreciated.
Full text: doi:10.1111/evo.13372
Recent theoretical models predict that the evolutionary diversification of the weapons and ornaments of pre-mating sexual selection should be influenced by trade-offs with male expenditure on ejaculates. However, the patterns of association between secondary sexual traits and ejaculate expenditure are frequently inconsistent in their support of this prediction. We show why con- sideration of additional life-history, ecological, and mating-system variables is crucial for the interpretation of associations between secondary sexual traits and ejaculate production. Incorporation of these 'missing variables' provides evidence that interactions between pre- and post-mating sexual selection can underlie broad patterns of diversification in male weapons and ornaments. We call for more experimental and genetic approaches to uncover trade-offs, as well as for studies that consider the costs of mate-searching.
Full text: doi:10.1016/j.tree.2017.09.011
Sexual selection theory predicts a trade-off between premating (ornaments and armaments) and postmating (testes and ejaculates) sexual traits, assuming that growing and maintaining these traits is costly and that total reproductive investments are limited. The number of males in competition, the reproductive gains from investing in premating sexual traits, and the level of sperm competition are all predicted to influence how males allocate their finite resources to these traits. Yet, empirical examination of these predictions is currently scarce. Here, we studied relative expenditure on pre- and postmating sexual traits among frog species varying in their population density, operational sex ratio and the number of competing males for each clutch of eggs. We found that the intensifying struggle to monopolize fertilizations as more and more males clasp the same female to fertilize her eggs shifts male reproductive investment toward sperm production and away from male weaponry. This shift, which is mediated by population density and the associated level of male-male competition, likely also explains the trade-off between pre- and postmating sexual traits in our much broader sample of anuran species. Our results highlight the power of such a multi-level approach in resolving the evolution of traits and allocation trade-offs.
Full text: doi:10.1111/evo.13246
Spermatozoa exhibit considerable interspecies morphological variation across mammals, especially among murid rodents. In Australasia, most murids in the tribe Hydromyini have a spermatozoon with a highly complex head exhibiting an apical hook, characteristic of most murids, and two projections that extend from its upper concave surface, the ventral processes. In the present study we performed a phylogenetically controlled comparison of sperm morphology across 45 species of hydromyine rodents to test the hypothesis that the length and angle of both the apical hook and ventral processes, as well as the length of the sperm tail, increase with relative testes mass as a proxy for differences in levels of inter-male sperm competition. Although both sperm head protrusions exhibited considerable variation in their length and angle across species, only the angles increased significantly in relation to relative testes mass. Further, the length of the sperm flagellum was positively associated with relative testes mass. These results suggest that, in hydromyine rodents, the angle of the apical hook and ventral processes of the sperm head, as well as the sperm tail length, are likely to be sexually selected traits. The possible functional significance of these findings is briefly discussed.
Full text: doi:10.1071/RD15425
Post-copulatory sexual selection (PSS), fuelled by female promiscuity, is credited with the rapid evolution of sperm quality traits across diverse taxa. Yet, our understanding of the adaptive significance of sperm ornaments and the cryptic female preferences driving their evolution is extremely limited. Here we review the evolutionary allometry of exaggerated sexual traits (for example, antlers, horns, tail feathers, mandibles, dewlaps), show that the giant sperm of some Drosophila species are possibly the most extreme ornaments in all of nature and demonstrate how their existence challenges theories explaining the intensity of sexual selection, mating-system evolution and the fundamental nature of sex differences. We also combine quantitative genetic analyses of interacting sex-specific traits in D. melanogaster with comparative analyses of the condition dependence of male and female reproductive potential across species with varying ornament size to reveal complex dynamics that may underlie sperm-length evolution. Results suggest that producing few gigantic sperm evolved by (1) Fisherian runaway selection mediated by genetic correlations between sperm length, the female preference for long sperm and female mating frequency, and (2) longer sperm increasing the indirect benefits to females. Our results also suggest that the developmental integration of sperm quality and quantity renders post-copulatory sexual selection on ejaculates unlikely to treat male-male competition and female choice as discrete processes.
Full text: doi:10.1038/nature18005
There is substantial comparative and growing experimental evidence that the competition for fertilization among sperm from different males can drive variation in male reproductive investments. However, less is known about the extent of natural variation in these investments relative to environmental variables affecting resource availability and mating system dynamics, which would allow insights into the mechanisms shaping reproductive allocation. Here, we studied interpopulation variation in male investments in testis size and sperm length across 25 populations of the Asian grass frog Fejervarya limnocharis along a 1550-km latitudinal and 1403-m altitudinal transect in China. We found relative testis mass and sperm length, male somatic condition, and the male/female sex ratio to increase with elevation but not latitude or longitude. Our results suggest that environmental variation may underlie local adaptations to reproductive investments among natural populations, mediated by differences in the availability of both resources and sexual partners (including the resulting male-male competition). These findings contrast with previous predictions that increasing latitude and/or elevation should lead to declining reproductive investments in male anurans due to shortening breeding seasons, declining resource availability, and lowering (rather than increasing) male/female sex ratios. We discuss these species differences in the context of differential resource allocation strategies, breeding ecology, and patterns of male-male competition. These differences show the need for future work on reproductive investments in anurans beyond the few model systems and for potential extension of the theoretical framework to species with different mating systems and strategies.
Full text: doi:10.1007/s00265-016-2128-9
Postcopulatory sexual selection is widely accepted to underlie the extraordinary diversification of sperm morphology. However, why does it favour longer sperm in some taxa but shorter in others? Two recent hypotheses addressing this discrepancy offered contradictory explanations. Under the spermdilution hypothesis, selection via spermdensity in the female reproductive tract favours more but smaller sperm in large, but the reverse in small, species. Conversely, the metabolic constraint hypothesis maintains that ejaculates respond positively to selection in small endothermic animals with high metabolic rates, whereas low metabolic rates constrain their evolution in large species. Here, we resolve this debate by capitalizing on the substantial variation inmammalian body size and reproductive physiology. Evolutionary responses shifted from sperm length to number with increasing mammalian body size, thus supporting the sperm dilution hypothesis. Our findings demonstrate that body-size-mediated trade-offs between sperm size and number can explain the extreme diversification in sperm phenotypes.
Full text: doi:10.1098/rspb.2015.2122
Males must carefully allocate the energy they devote to sex. A new study of howler monkeys shows that males who use vocalizations to ward off rivals invest less in producing large numbers of sperm.
Full text: doi:10.1016/j.cub.2015.09.060
Male ornaments and armaments that mediate success in mate acquisition and ejaculate traits influencing competitive fertilization success are under intense sexual selection. However, relative investment in these pre- and post-copulatory traits depends on the relative importance of either selection episode and on the energetic costs and fitness gains of investing in these traits. Theoretical and empirical work has improved our understanding of how precopulatory sexual traits and investments in sperm production covary in this context. It has recently also been suggested that male weapon size may trade off with sperm length as another post-copulatory sexual trait, but the theoretical framework for this suggestion remains unclear. We evaluated the relationship between precopulatory armaments and sperm length, previously reported in ungulates, in five taxa as well as meta-analytically. Within and between taxa, we found no evidence for a negative or positive relationship between sperm length and male traits that are important in male-male contest competition. It is important to consider pre- and post-copulatory sexual selection together to understand fitness, and to study investments in different reproductive traits jointly rather than separately. A trade-off between pre- and post-copulatory sexual traits may not manifest itself in sperm length but rather in sperm number or function. Particularly in large-bodied taxa such as ungulates, sperm number is more variable interspecifically and likely to be under more intense selection than sperm length. We discuss our and the previous results in this context.
Full text: doi:10.1111/jeb.12742
Many songbirds are socially monogamous but genetically polyandrous, mating with individuals outside their pair bonds. Extra-pair paternity (EPP) varies within and across species, but reasons for this variation remain unclear. One possible source of variation is population genetic diversity, which has been shown in interspecific meta-analyses to correlate with EPP but which has limited support from intraspecific tests. Using eight populations of the genetically polyandrous red-winged blackbird (Agelaius phoeniceus), including an island population, we investigated whether population-level differences in genetic diversity led to differences in EPP. We first measured genetic diversity over 10 microsatellite loci and found, as predicted, low genetic diversity in the island population. Additional structure analyses with multilocus genotypes and mtDNA showed the island population to be distinct from the continental populations. However, the island population's EPP rate fell in the middle of the continental populations' distribution, whereas the continental populations themselves showed significant variation in EPP. This result suggests that genetic diversity by itself is not a predictor of EPP rate. We discuss reasons for the departure from previous results, including hypotheses for EPP that do not solely implicate female-driven behaviour.
Full text: doi:10.1111/jeb.12644
Sperm experience intense and varied selection that dramatically impacts the evolution of sperm quality. Selection acts to ensure that sperm are fertilization-competent and able to overcome the many challenges experienced on their way towards eggs. However, simply being able to fertilize an egg is not enough to ensure male fertility in most species. Owing to the prevalence of female multiple mating throughout the animal kingdom, successful fertilization requires sperm to outcompete rival sperm. In addition, females can actively influence sperm quality, storage or utilization to influence male fertility. This review provides an overview of how these selective forces influence the evolution of sperm quality. After exploring the link between sperm traits and male fertility, we examine how post-mating competition between rival ejaculates influences the evolution of sperm quality. We then describe how complex genetic, social and sexual interactions influence sperm quality, focusing on the importance of seminal fluid and interactions between sperm and the female's reproductive tract. In light of the complexities of selection on sperm traits, greater use of multivariate approaches that incorporate male-male, sperm-sperm and sperm-female interactions to study sperm quality will enhance our understanding of how selection acts on sperm traits and factors influencing male fertility. Because the metric of male reproductive success - fertilization - is the same across the animal kingdom, we argue that information about sperm evolution gained from non-human animals has enormous potential to further our understanding of the factors that impact human fertility.
Full text: doi:10.1093/molehr/gau067
Theory predicts a trade-off between investments in precopulatory (ornaments and armaments) and postcopulatory (testes and ejaculates) sexual traits due to the costs associated with their growth and maintenance within the finite energy resources available. Empirical studies, however, have revealed considerable inconsistency in the strength and direction of relationships among these sexual traits. Ambiguity may result from variance in the marginal benefits gained by increasing investments in either pre- or postcopulatory sexual traits. Here, in a broad comparative study, we test the prediction that the relationship between pre- and postcopulatory sexual traits differs among taxa relative to the importance of male-male contest competition within them. We find that covariance between pre- and postcopulatory sexual traits gradually shifts from strongly positive to strongly negative with increasing male-male contest competition. Thus, our findings reveal a potentially unifying explanation for the oftentimes inconsistent relationships in the strength and direction of covariance among sexual traits.
Full text: doi:10.1038/ncomms4184
Mating between relatives usually decreases genetic quality of progeny as deleterious recessive alleles are expressed in inbred individuals. Inbreeding degrades sperm traits but its effects on sperm storage and fate within females are currently unknown. We quantified the relationship between the degrees of inbreeding relevant to natural populations (f=0, 0.25 and 0.50) and the number of sperm inseminated and stored, sperm swimming speed, long-term sperm viability while in storage, pattern of sperm precedence, mating latency, and offspring viability of female Drosophila melanogaster. The use of transgenic flies that have either red or green fluorescent sperm heads allowed us to distinguish two ejaculates in the female reproductive tract and facilitated quantification of sperm storage and use traits. We found no inbreeding depression in either long- or short-term sperm storage ability. The most inbred females exhibited significantly longer mating latency, which could be explained by males preferring to mate with outbred females. On the other hand, as no evidence for cryptic male choice in the form of ejaculate tailoring of sperm number was found, the most inbred females might just be less eager to mate. We also found no evidence that the degree of maternal inbreeding influenced offspring viability. Comparison with a contemporaneous study of male inbreeding consequences for ejaculate quality suggests that inbreeding depression is more severe in males than in females in our study population.
Full text: doi:10.1016/j.jinsphys.2013.10.005
Recent work suggests that the yellow dung fly mating system may include alternative patroller-competitor mating tactics in which large males compete for gravid females on dung, whereas small, non-competitive males search for females at foraging sites. Small males obtain most matings off pasture, yet the behavioural mechanism(s) giving rise to this pattern are unknown. We investigated the male and female behaviours that determine mating success in this environment by conducting field mating experiments and found small males to benefit from several attributes specific to the off-pasture mating environment. First, small males from foraging sites exhibited higher mating propensity, indicating that large males away from dung may be depleted of energy and/or sperm. Second, small males were more discriminating, being significantly less likely to attempt with non-gravid females, which are absent on dung but common off pasture. Third, non-gravid females were generally more likely to actively struggle and reject mating attempts; however, such behaviours occurred disproportionately more often with large males. Female Scathophaga stercoraria thus appear to preferentially mate with small males when off pasture. These findings challenge assumptions about male-female interactions in systems with alternative mating tactics and reveal hidden processes that may influence selection patterns in the field.
Full text: doi:10.1098/rspb.2013.2164
BACKGROUND: Identifying traits that reproductively isolate species, and the selective forces underlying their divergence, is a central goal of evolutionary biology and speciation research. There is growing recognition that postcopulatory sexual selection, which can drive rapid diversification of interacting ejaculate and female reproductive tract traits that mediate sperm competition, may be an engine of speciation. Conspecific sperm precedence (CSP) is a taxonomically widespread form of reproductive isolation, but the selective causes and divergent traits responsible for CSP are poorly understood.
RESULTS: To test the hypothesis that postcopulatory sexual selection can generate reproductive isolation, we expressed GFP or RFP in sperm heads of recently diverged sister species, Drosophila simulans and D. mauritiana, to enable detailed resolution of species-specific sperm precedence mechanisms. Between-species divergence in sperm competition traits and mechanisms prompted six a priori predictions regarding mechanisms of CSP and degree of cross asymmetry in reproductive isolation. We resolved four distinct mechanisms of CSP that were highly consistent with predictions. These comprise interactions between multiple sex-specific traits, including two independent mechanisms by which females exert sophisticated control over sperm fate to favor the conspecific male.
CONCLUSIONS: Our results confirm that reproductive isolation can quickly arise from diversifying (allopatric) postcopulatory sexual selection. This experimental approach to "speciation phenotypes" illustrates how knowledge of sperm precedence mechanisms can be used to predict the mechanisms and extent of reproductive isolation between populations and species.
Full text: doi:10.1016/j.cub.2013.07.086
How females store and use sperm after remating can generate postcopulatory sexual selection on male ejaculate traits. Variation in ejaculate performance traits generally is thought to be intrinsic to males but is likely to interact with the environment in which sperm compete (e.g., the female reproductive tract). Our understanding of female contributions to competitive fertilization success is limited, however, in part because of the challenges involved in observing events within the reproductive tract of internally fertilizing species while discriminating among sperm from competing males. Here, we used females from crosses among isogenic lines of Drosophila melanogaster, each mated to two genetically standardized males (the first with green- and the second with red-tagged sperm heads) to demonstrate heritable variation in female remating interval, progeny production rate, sperm-storage organ morphology, and a number of sperm performance, storage, and handling traits. We then used multivariate analyses to examine relationships between this female-mediated variation and competitive paternity. In particular, the timing of female ejection of excess second-male and displaced first-male sperm was genetically variable and, by terminating the process of sperm displacement, significantly influenced the relative numbers of sperm from each male competing for fertilization, and consequently biased paternity. Our results demonstrate that females do not simply provide a static arena for sperm competition but rather play an active and pivotal role in postcopulatory processes. Resolving the adaptive significance of genetic variation in female-mediated mechanisms of sperm handling is critical for understanding sexual selection, sexual conflict, and the coevolution of male and female reproductive traits.
Full text: doi:10.1073/pnas.1300954110
Directional dominance is a prerequisite of inbreeding depression. Directionality arises when selection drives alleles that increase fitness to fixation and eliminates dominant deleterious alleles, while deleterious recessives are hidden from it and maintained at low frequencies. Traits under directional selection (i.e., fitness traits) are expected to show directional dominance and therefore an increased susceptibility to inbreeding depression. In contrast, traits under stabilizing selection or weakly linked to fitness are predicted to exhibit little-to-no inbreeding depression. Here, we quantify the extent of inbreeding depression in a range of male reproductive characters and then infer the mode of past selection on them. The use of transgenic populations of Drosophila melanogaster with red or green fluorescent-tagged sperm heads permitted in vivo discrimination of sperm from competing males and quantification of characteristics of ejaculate composition, performance, and fate. We found that male attractiveness (mating latency) and competitive fertilization success (P2) both show some inbreeding depression, suggesting they may have been under directional selection, whereas sperm length showed no inbreeding depression suggesting a history of stabilizing selection. However, despite having measured several sperm quality and quantity traits, our data did not allow us to discern the mechanism underlying the lowered competitive fertilization success of inbred (f = 0.50) males.
Full text: doi:10.1002/ece3.625
How sperm from competing males are used to fertilize eggs is poorly understood yet has important implications for postcopulatory sexual selection. Sperm may be used in direct proportion to their numerical representation within the fertilization set or with a bias toward one male over another. Previous theoretical treatments have assumed a single sperm-storage organ, but many taxa possess multiple organs or store sperm within multiple regions of the reproductive tract. In Drosophila, females store sperm in two distinct storage organ types: the seminal receptacle (SR) and the paired spermathecae. Here, we expand previous "raffle" models to describe "fertilization bias" independently for sperm within the SR and the spermathecae and estimate the fertilization set based on the relative contribution of sperm from the different sperm-storage organ types. We apply this model to three closely related species to reveal rapid divergence in the fertilization set and the potential for female sperm choice.
Full text: doi:10.1086/671782
The outcome of sperm competition is influenced by the relative quantity and quality of sperm among competing ejaculates. Whereas it is well established that individual ejaculate traits evolve rapidly under postcopulatory sexual selection, little is known about other factors that might influence the evolution of ejaculates. For example, the metabolic rate is likely to affect the sperm production rate and the cellular activity or metabolism of sperm, and it has recently been suggested to constrain the evolution of sperm length in large but not small mammals. I thus examined in eutherian mammals how ejaculate quality traits vary with one another and with testis mass, body size, and metabolism. I found all ejaculate traits to covary positively with one another and to increase with relative testis mass. When controlling for testis mass, small-bodied species showed superior sperm quality (but not sperm number). Furthermore, sperm motility and viability were positively associated with the mass-corrected metabolic rate, but the percentage of morphologically normal and acrosome-intact sperm were not. These results indicate that body size and the energy budget may also influence the evolution of ejaculate quality, although these influences appear to vary among traits.
Full text: doi:10.1111/evo.12132
Postcopulatory sexual selection is credited with driving rapid evolutionary diversification of reproductive traits and the formation of reproductive isolating barriers between species. This judgment, however, has largely been inferred rather than demonstrated due to general lack of knowledge about processes and traits underlying variation in competitive fertilization success. Here, we resolved processes determining sperm fate in twice-mated females, using transgenic Drosophila simulans and Drosophila mauritiana populations with fluorescently labeled sperm heads. Comparisons among these two species and Drosophila melanogaster revealed a shared motif in the mechanisms of sperm precedence, with postcopulatory sexual selection potentially occurring during any of the three discrete stages: (1) insemination; (2) sperm storage; and (3) sperm use for fertilization, and involving four distinct phenomena: (1) sperm transfer; (2) sperm displacement; (3) sperm ejection; and (4) sperm selection for fertilizations. Yet, underlying the qualitative similarities were significant quantitative differences in nearly every relevant character and process. We evaluate these species differences in light of concurrent investigations of within-population variation in competitive fertilization success and postmating/prezygotic reproductive isolation in hybrid matings between species to forge an understanding of the relationship between microevolutionary processes and macroevolutionary patterns as pertains to postcopulatory sexual selection in this group.
Full text: doi:10.1111/evo.12117
Post-copulatory sexual selection arises when females mate with multiple males, resulting in competition between ejaculates to fertilize the female's eggs. Such selection is recognized as an important engine of evolutionary diversification and speciation, yet the mechanisms underlying sperm competition are poorly known due to dual challenges of observing events within the female reproductive tract and of discriminating the sperm of different males. Use of Drosophila melanogaster and related species with GFP- or RFP-labeled protamine in sperm heads has enabled real-time and spatiotemporal analyses of in vivo sperm behavior and fate. Here, the 10.5-μm long sperm heads are visible (but not the roughly 1850-μm long flagella) within the primary sperm-storage organ, the seminal receptacle, of a twice-mated female. After re-mating, the second-male sperm (in this instance, red) begin to enter the storage organs and physically displace resident (green) sperm, resulting in a predominance of sperm from the recent mate. This process continues until the female forcibly ejects all excess second-male and displaced first-male sperm from her uterus. Studies with these lines have revealed that sperm exhibit a surprisingly complex behavioral repertoire, and that longer and slower sperm are superior at displacing, and resisting displacement by, faster and shorter sperm.
Full text: doi:10.1002/mrd.22155
Many reproductive traits, including ejaculate characteristics, usually show remarkable seasonal variation, but the potential for such dynamics in sperm morphology has been overlooked. Several studies have revealed high within-male repeatability in sperm morphology, but samples have typically been collected within a few hours or days, and the consistency of sperm morphology over longer periods remains unexplored. Here, we tested whether ejaculate traits, including sperm morphology, sperm number, and sperm velocity, exhibit seasonal phenotypic plasticity in a long-lived seasonal breeder, the red-winged blackbird (Agelaius phoeniceus). We found absolute and/or relative flagellum length and sperm velocity to increase across the season, whereas sperm numbers within ejaculates declined. Sperm morphological traits were further positively associated with harem size or the total number of offspring that fledged in each male's territory, suggesting that sperm morphology is likely to be linked to male reproductive quality. The underlying mechanisms of these patterns of seasonal variation remain unresolved, but we discuss our results in the context of dynamics of reproductive hormones, testicular structures and function, and reproductive behavior.
Full text: doi:10.1007/s00265-012-1415-3
Success in sperm competition, occurring whenever females mate with multiple males, is predicted to be influenced by variation in ejaculate quality and interactions among competing sperm. Yet, apart from sperm number, relevant ejaculate characteristics and sperm-sperm interactions are poorly understood, particularly within a multivariate framework and the natural selective environment of the female reproductive tract. Here, we used isogenic lines of Drosophila melanogaster with distinguishable sperm to demonstrate and partition genetic variation in multiple sperm quality and performance traits. Next, by competing males from different lines, we show how rival sperm significantly influence each other's velocity and reveal that males with relatively slow and/or long sperm better displace rival sperm and resist displacement, thus avoiding ejection by the female from her reproductive tract. Finally, we establish fitness consequences of genetic variation in sperm quality and its role in securing a numerical advantage in storage by showing that offspring paternity is determined strictly by the representation of stored, competing sperm. These results provide novel insight into complex postcopulatory processes, illustrate that different ejaculate traits are critical at different biologically relevant time-points, and provide a critical foundation for elucidating the role of postcopulatory sexual selection in trait diversification and speciation.
Full text: doi:10.1016/j.cub.2012.06.059
In polyandrous mating systems, male fitness depends on success in premating, post-copulatory and offspring viability episodes of selection. We tracked male success across all of these episodes simultaneously, using transgenic Drosophila melanogaster with ubiquitously expressed green fluorescent protein (i.e. GFP) in a series of competitive and noncompetitive matings. This approach permitted us to track paternity-specific viability over all life stages and to distinguish true competitive fertilization success from differential early offspring viability. Relationships between episodes of selection were generally not present when paternity was measured in eggs; however, positive correlations between sperm competitive success and offspring viability became significant when paternity was measured in adult offspring. Additionally, we found a significant male x female interaction on hatching success and a lack of repeatability of offspring viability across a focal male's matings, which may underlay the limited number of correlations found between episodes of selection.
Full text: doi:10.1111/j.1420-9101.2012.02540.x
Sperm biology pervades numerous research areas from clinical research to evolutionary biology and animal conservation. Integrating these fields for a better understanding of each is one of the main goals of the Biology of Spermatozoa meeting, a conference held biennially outside of Sheffield in the United Kingdom. This September, at the 11th meeting, scientists from around the globe presented their ongoing research on numerous aspects of reproductive biology, from assisted reproduction in humans and animal conservation through stem cell research and proteomics to sophisticated evolutionary adaptations of ejaculates and female reproductive traits in order to bias paternity toward one or the other male in situations of female promiscuity. Throughout the conference, ethical controversies with reproductive applications (e.g., sperm banking) found their place just as much as novel clinical technologies (e.g., sperm quality assays) or major advances in understanding the mechanisms underlying fundamental processes of postcopulatory sexual selection (e.g., using transgenic animals that produce fluorescently labeled sperm). Across a wide range of different taxa, this meeting has presented a fascinating synthesis of current research and emerging directions in the study of sperm biology.
Full text: doi:10.4161/spmg.1.4.18327
Selection to avoid inbreeding is predicted to vary across species due to differences in population structure and reproductive biology. Over the past decade, there have been numerous investigations of postcopulatory inbreeding avoidance, a phenomenon that first requires discrimination of mate (or sperm) relatedness and then requires mechanisms of male ejaculate tailoring and/or cryptic female choice to avoid kin. The number of studies that have found a negative association between male-female genetic relatedness and competitive fertilization success is roughly equal to the number of studies that have not found such a relationship. In the former case, the underlying mechanisms are largely unknown. The present study was undertaken to verify and expand upon a previous report of postcopulatory inbreeding avoidance in D. melanogaster, as well as to resolve underlying mechanisms of inbreeding avoidance using transgenic flies that express a sperm head-specific fluorescent tag. However, siblings did not have a lower fertilization success as compared to unrelated males in either the first (P(1) ) or second (P(2) ) mate role in sperm competition with a standard unrelated competitor male in our study population of D. melanogaster. Analyses of mating latency, copulation duration, egg production rate, and remating interval further revealed no evidence for inbreeding avoidance.
Full text: doi:110.1111/j.1558-5646.2011.01317.x
Spermatozoa are amongst the most variable cells, and three factors are thought to account for this variation in design: fertilization mode, phylogeny, and postcopulatory sexual selection. In addition, it has long been assumed that a tradeoff exists between sperm size and number, and although postcopulatory sexual selection affects both traits, empirical evidence for a tradeoff has so far been elusive. Our recent theoretical model predicts that the nature of a direct tradeoff between sperm size and number varies with sperm competition mechanism and sperm competition risk. We test these predictions using a comparative approach in two very different taxa with different sperm competition mechanisms: passerine birds (mechanism: simple raffle) and Drosophila fruit flies (sperm displacement). We show that in both groups, males increase their total ejaculate investment with increasing sperm competition risk, but whereas passerine birds allocate disproportionately to sperm number, drosophilids allocate disproportionately to sperm size. This striking difference between the two groups can be at least partly explained by sperm competition mechanisms depending on sperm size relative to the size of the female reproductive tract: in large animals (passerines), sperm numbers are advantageous in sperm competition owing to dilution inside the female tract, whereas in small animals (drosophilids), large sperm are advantageous for physical competition (sperm displacement). Our study provides two important results. First, we provide convincing evidence for the existence of a sperm size-number tradeoff. Second, we show that by considering both sperm competition mechanism and dilution, can we account for variation in sperm size between different taxa.
Full text: doi:10.1073/pnas.1009059108
The outcome of sperm competition (i.e. competition for fertilization between ejaculates from different males) is primarily determined by the relative number and quality of rival sperm. Therefore, the testes are under strong selection to maximize both sperm number and quality, which are likely to result in trade-offs in the process of spermatogenesis (e.g. between the rate of spermatogenesis and sperm length or sperm energetics). Comparative studies have shown positive associations between the level of sperm competition and both relative testis size and the proportion of seminiferous (sperm-producing) tissue within the testes. However, it is unknown how the seminiferous tissue itself or the process of spermatogenesis might evolve in response to sperm competition. Therefore, we quantified the different germ cell types and Sertoli cells (SC) in testes to assess the efficiency of sperm production and its associations with sperm length and mating system across 10 species of New World Blackbirds (Icteridae) that show marked variation in sperm length and sperm competition level. We found that species under strong sperm competition generate more round spermatids (RS)/spermatogonium and have SC that support a greater number of germ cells, both of which are likely to increase the maximum sperm output. However, fewer of the RS appeared to elongate to mature spermatozoa in these species, which might be the result of selection for discarding spermatids with undesirable characteristics as they develop. Our results suggest that, in addition to overall size and gross morphology, testes have also evolved functional adaptations to maximize sperm quantity and quality.
Full text: doi:10.1530/REP-10-0501
In contrast to early predictions, it is now widely accepted that males incur substantive costs from ejaculate production. Hence, males are predicted to allocate their reproductive investments, including ejaculate size, relative to the risk of sperm competition and to female quality. The study of sperm allocation, however, has been technically challenging with nonvirgin females because sperm fromdifferent males must be discriminated within the female reproductive tract. To date, such investigations have thus largely been restricted to species that transfer sperm in spermatophores or for which females can be fitted with a harness to capture the incoming ejaculate. In this study, we examined sperm allocation using male Drosophila melanogaster that express a fluorescently labeled protein in sperm heads, allowing us to quantify sperm numbers from different males within the female reproductive tract. We found that male D. melanogaster deliver significantly more sperm to mated, large or young females compared with virgins, small or old females, respectively, whereas copulation duration was only significantly longer with large than with small females. These results provide further evidence for costly ejaculate production and consequent prudent allocation of sperm.
Full text: doi:10.1093/beheco/arq193
Cellular membranes are composed of highly variable lipid molecules, mainly cholesterol and phospholipids (PLs). The cholesterol moiety and the saturation degree of the fatty acyl residues of PL determine the fluidity of the membrane, which is particularly important for sperm because they have to undergo characteristic membrane-dependent processes (acrosomal exocytosis and fusion with the oocyte). Glycolipids are an essential part of the membrane surface acting as key mediators in the interactions of sperm with components of the female genital tract. Although the lipid composition of many mammalian spermatozoa has already been determined, the lipid composition of avian spermatozoa has scarcely been investigated. Using spermatozoa extracts of the ring-necked pheasant (Phasianus colchicus) as a selected example, this work demonstrates that matrix-assisted laser desorption and ionization time-of-flight mass spectrometry (MALDI-TOF MS) is a simple and fast method to determine spermatozoal lipid compositions. The lipid compositions of pheasant spermatozoa have not yet been investigated. In addition to common membrane (primarily diacyl) PL (sphingomyelin, phosphatidylcholine, phosphatidylinositol and phosphatidylethanolamine), remarkable variation of different sulfoglycolipids (sulfogalactocerebrosides) was identified. This is in strong contrast to all other animal species investigated so far which nearly exclusively contain the sulfoglycolipid seminolipid (sulfogalactoalkylacylglycerol). We emphasize that the MALDI MS approach allows the characterization of sulfoglycolipids of sperm within a few minutes without the necessity for previous chromatographic separation.
Full text: doi:10.1016/j.anireprosci.2011.01.009
Many species differ genetically, physiologically, and morphologically between geographically distinct populations, typically in response to variation in ecological and climatic variables. Little is known, however, about geographical variation in sperm morphology. Sperm morphology is under strong sexual selection, has been shown to evolve rapidly, and often co-varies with other reproductive traits (e.g., testis size or mating system) that differ between populations in some species. The aim of this study was to establish whether sperm morphology varies between populations of the red-winged blackbird (Agelaius phoeniceus), a species with an enormous breeding range and marked inter-population variation in both body size and mating system. We found (1) highly significant variation in sperm morphology among study sites, (2) a gradual increase in sperm length from the southwest to the northeast of the breeding range, and (3) a strong negative association between sperm length and body size. However, the relationship with the mating system remains unclear. Several hypotheses to explain these patterns are proposed.
Full text: doi:10.1007/s10682-010-9410-5
Sperm velocity is one of the main determinants of the outcome of sperm competition. Since sperm vary considerably in their morphology between and within species, it seems likely that sperm morphology is associated with sperm velocity. Theory predicts that sperm velocity may be increased by enlarged midpiece (energetic component) or flagellum length (kinetic component), or by particular ratios between sperm components, such as between flagellum length and head size. However, such associations have rarely been found in empirical studies. In a comparative framework in passerine birds, we tested these theoretical predictions both across a wide range of species and within a single family, the New World blackbirds (Icteridae). In both study groups, sperm velocity was influenced by sperm morphology in the predicted direction. Consistent with theoretical models, these results show that selection on sperm morphology and velocity are likely to be concomitant evolutionary forces.
Full text: doi:10.1098/rspb.2008.1645
Post-copulatory sexual selection (PCSS) is thought to be one of the evolutionary forces responsible for the rapid and divergent evolution of sperm design. However, whereas in some taxa particular sperm traits are positively associated with PCSS, in other taxa, these relationships are negative, and the causes of these different patterns across taxa are poorly understood. In a comparative study using New World blackbirds (Icteridae), we tested whether sperm design was influenced by the level of PCSS and found significant positive associations with the level of PCSS for all sperm components but head length. Additionally, whereas the absolute length of sperm components increased, their variation declined with the intensity of PCSS, indicating stabilising selection around an optimal sperm design. Given the diversity of, and strong selection on, sperm design, it seems likely that sperm phenotype may influence sperm velocity within species. However, in contrast to other recent studies of passerine birds, but consistent with several other studies, we found no significant link between sperm design and velocity, using four different species that vary both in sperm design and PCSS. Potential reasons for this discrepancy between studies are discussed.
Full text: doi:10.1007/s00265-009-0733-6
Sperm morphology varies considerably across taxa, and postcopulatory sexual selection is thought to be one of the main forces responsible for this diversity. Several studies have investigated the effects of the variation in sperm design on sperm function, but the consequences of variation in sperm design on testis morphology have been overlooked. Testes size or architecture may determine the size of the sperm they produce, and selection for longer sperm may require concomitant adaptations in the testes. Relative testes size differs greatly between species and is often used as an index of sperm competition, but little is known about whether larger testes have more sperm-producing tissue or produce sperm at a faster rate. Using a comparative approach in New World Blackbirds (Icteridae), we found (1) a strong link between testis histology and sperm length, suggesting selection on testis architecture through selection on sperm size, and (2) that species under intense sperm competition had a greater proportion of sperm-producing tissue within their testes. These results support the prediction that sperm competition fosters adaptations in reproductive organs that extend beyond testes size, and raise questions about the trade-offs influencing reproductive investment.
Full text: doi:10.1111/j.1558-5646.2008.00571.x
Male genitalia are typically highly variable across species, for which sexual selection is thought to be responsible. Sexually selected traits characteristically show positive allometry and high phenotypic variation, although genitalia seem to be typified by negative allometry due to stabilizing selection. Additionally, while sexual selection appears to be the primary force responsible for genital evolution, the precise mechanism is unclear, but good-genes selection could be involved. If so, male genital variation should correlate with some male quality measure(s). We investigated the allometry of male Nyctalus noctula genitalia and investigated associations between genital size and three phenotypic measures of male quality (body size, relative body mass, and fluctuating asymmetry (FA)). We found that the penis exhibited positive allometry and high phenotypic variation, and was positively associated with male body size and relative body mass, but not with FA. This pattern is more typical of sexually selected display traits, contrasting with general patterns of genital allometry. The baculum was negatively allometric and was not associated with any quality measure. Our results suggest that the N. noctula penis is under directional sexual selection and is a reliable indicator of male phenotypic quality.
Full text: doi:10.1111/j.1095-8312.2004.00407.x
Although sociality is common in bats, few studies have investigated individual social behaviour in free-ranging colonies. This study quantifies social interactions among wild female Bechstein's bats (Myotis bechsteinii) belonging to one maternity colony. Our main goal was to analyse allogrooming and nose rubbing, which are both regularly displayed by adult females. Based on data of individually marked bats with known degrees of pairwise relatedness, we suggest that allogrooming has both a social and a hygienic function. Females groomed colony mates mainly on parts of the body that are difficult to reach by a bat itself. Thus, allogrooming may function to remove ectoparasites from inaccessible body parts. Allogrooming was rare compared to self-grooming (on average 0.7% vs 37.7% of a female's total observation time), and there was no significant correlation between the rate at which a bat groomed itself and the frequency with which it was groomed by conspecifics. Therefore, we assume that allogrooming also has a social purpose in addition to its assumed hygienic function. We suggest that allogrooming could strengthen social bonds among colony members that live together for many years. Mothers and adult daughters groomed each other preferentially. Thus, allogrooming may reflect special mother–daughter bonds. Nose rubbing occurred mainly within minutes (median: 80 s) after the arrival of a female in a night roost, and there was no correlation with relatedness. Therefore, it probably allows recognition of colony mates and may also be a greeting behaviour.
Full text: doi:10.1007/s10211-003-0075-8
Tadpoles of many species develop enlarged tail fins in the presence of insect predators, but the function of this response is not known. Because large tails do not improve swimming performance, we tested the hypothesis that the tail attracts predator strikes away from the more vulnerable head and body region. We first confirmed the assumption that attacks to the tail are less dangerous: Living tadpoles escaped from dragonfly larvae only 10% of the time when the strike landed on the head and body but 29.4% of the time when struck on the tail. We then constructed model tadpoles having four tail shapes: normal, predator-induced, and 50% shallower and 50% deeper than normal. The models were presented to dragonflies and the location at which the insect's labium struck the model was noted. Models having the predator-induced tail sustained 16% fewer strikes to the head and body than did models with the noninduced tail, lending credibility to the hypothesis that the tail acts as a lure. Models with an unnaturally large tail were attacked more often on the body than was the predator-induced model, which may create stabilizing selection on tail shape.