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opencc-zeroDec 2018View details →

Data from: Conspecific sperm precedence is reinforced, but postcopulatory sexual selection weakened, in sympatric populations of Drosophila

Sexual selection can accelerate speciation by driving the evolution of reproductive isolation, but forces driving speciation could also reciprocally feedback on sexual selection. This might be particularly important in the context of 'reinforcement', where selection acts directly to increase prezygotic barriers to reduce the cost of heterospecific matings. Using assays of sperm competition within and between two sister species, we show a signature of reinforcement where these species interact: populations of Drosophila pseudoobscura that co-occur with sister species D. persimilis have an elevated ability to outcompete heterospecific sperm, consistent with selection for increased postcopulatory isolation. We also find these D. pseudoobscura populations have decreased sperm competitive ability against conspecifics, reducing the opportunity for sexual selection within these populations. Our findings demonstrate that direct selection to increase reproductive isolation against other species can compromise the efficacy of sexual selection within species, a collateral effect of reproductive traits responding to heterospecific interactions.

Data from: Cryptic female choice favours sperm from MHC-dissimilar males

Cryptic female choice may enable polyandrous females to avoid inbreeding or bias offspring variability at key loci after mating. However, the role of these genetic benefits in cryptic female choice remains poorly understood. Female red junglefowl, Gallus gallus, bias sperm use in favour of unrelated males. Here, we experimentally investigate whether this bias is driven by relatedness per se, or by similarity at the major histocompatibility complex (MHC), genes central to vertebrate acquired immunity, where polymorphism is critical to an individual's ability to combat pathogens. Through experimentally controlled natural matings, we confirm that selection against related males' sperm occurs within the female reproductive tract but demonstrate that this is more accurately predicted by MHC similarity: controlling for relatedness per se, more sperm reached the eggs when partners were MHC-dissimilar. Importantly, this effect appeared largely owing to similarity at a single MHC locus (class I minor). Further, the effect of MHC similarity was lost following artificial insemination, suggesting that male phenotypic cues might be required for females to select sperm differentially. These results indicate that postmating mechanisms that reduce inbreeding may do so as a consequence of more specific strategies of cryptic female choice promoting MHC diversity in offspring.

Data from: A trade-off between thickness and length in the zebra finch sperm mid-piece

The sperm mid-piece has traditionally been considered to be the engine that powers sperm. Larger mid-pieces have therefore been assumed to provide greater energetic capacity. However, in the zebra finch Taeniopygia guttata, a recent study showed a surprising negative relationship between mid-piece length and sperm energy content. Using a multidimensional approach to study mid-piece structure, we tested whether this unexpected relationship can be explained by a trade-off between mid-piece length and mid-piece thickness and/or cristae density inside the mitochondrial helix. We used selective plane illumination microscopy to study mid-piece structure from three-dimensional images of zebra finch sperm and used high-resolution transmission electron microscopy to quantify mitochondrial density. Contrary to the assumption that longer mid-pieces are larger and therefore produce or contain a greater amount of energy, our results indicate that the amount of mitochondrial material is consistent across mid-pieces of varying lengths, and longer mid-pieces are simply proportionately 'thinner'.

Data from: No association between sperm competition and sperm length variation across dung flies (Scathophagidae)

Sperm length is extremely variable across species, but a general explanation for this variation is lacking. However, when the risk of sperm competition is high, sperm length is predicted to be less variable within species, and there is some evidence for this in birds and social insects. Here, we examined intraspecific variation in sperm length, both within and between males, and its potential associations with sperm competition risk and variation in female reproductive tract morphology across dung flies. We used two measures of variation in sperm size, and testis size was employed as our index of sperm competition risk. We found no evidence of associations between sperm length variation and sperm competition or female reproductive tract variation. These results suggest that variation in sperm competition risk may not always be associated with variation in sperm morphology, and the cause(s) of sperm length variation in dung flies remains unclear.

opencc-zeroDec 2018View details →

Data from: Male responses to sperm competition risk when rivals vary in their number and familiarity

Males of many species adjust their reproductive investment to the number of rivals present simultaneously. However, few studies have investigated whether males sum previous encounters with rivals, and the total level of competition has never been explicitly separated from social familiarity. Social familiarity can be an important component of kin recognition and has been suggested as a cue that males use to avoid harming females when competing with relatives. Previous work has succeeded in independently manipulating social familiarity and relatedness among rivals, but experimental manipulations of familiarity are confounded with manipulations of the total number of rivals that males encounter. Using the seed beetle Callosobruchus maculatus we manipulated three factors: familiarity among rival males, the number of rivals encountered simultaneously, and the total number of rivals encountered over a 48-hour period. Males produced smaller ejaculates when exposed to more rivals in total, regardless of the maximum number of rivals they encountered simultaneously. Males did not respond to familiarity. Our results demonstrate that males of this species can sum the number of rivals encountered over separate days, and therefore the confounding of familiarity with the total level of competition in previous studies should not be ignored.

Data from: A sex-linked supergene controls sperm morphology and swimming speed in a songbird

Sperm are perhaps the most diverse cells in the animal kingdom, with enormous morphological variation between taxa, between species, between males and within an ejaculate. Considerable interest in sperm diversity has arisen following the realisation that sperm competition (post-copulatory sexual selection) is a powerful selective force in many organisms, and that sperm morphology has co-evolved with female reproductive tract morphology. However, the relationship between sperm morphology, sperm motility and fertilisation success is only partially understood. The extent to which between-male variation is heritable is largely unknown, and remarkably few studies have investigated the genetic architecture of sperm traits, especially sperm morphology. Here we use high-density genotyping and gene expression profiling to explore the considerable sperm trait variation that exists in the zebra finch Taeniopygia guttata. We show that nearly all of the genetic variation in sperm morphology is caused by an inversion polymorphism on the Z chromosome acting as a 'supergene'. These results provide a striking example of two evolutionary genetic predictions. First, that in species where females are the heterogametic sex, genetic variation affecting sexually dimorphic traits will accumulate on the Z chromosome. Second, recombination suppression at the inversion allows beneficial dominant alleles to become fixed on whichever haplotype they first arise, without being exchanged onto other haplotypes. Finally, we show that the inversion polymorphism will be stably maintained by heterozygote advantage, because heterozygous males have the fastest and most successful sperm with no apparent fitness cost.

opencc-zeroOct 2019View details →

Complex interactions between sperm viability and female fertility

<p>Sperm viability is a major male fitness component, with higher sperm viability associated with enhanced sperm competitiveness. While many studies have focussed on sperm viability from the male fitness standpoint, its impact on female fitness is less clear. Here we used a panel of 32 isogenic <i>Drosophila simulans</i> lines to test for genetic variation in sperm viability (percentage of viable cells). We then tested whether sperm viability affected female fitness by mating females to males from low or high sperm viability genotypes. We found significant variation in sperm viability among genotypes, and consistent with this, sperm viability was highly repeatable within genotypes. Additionally, females mated to high sperm viability males laid more eggs in the first seven hours after mating, and produced more offspring in total. However, the early increase in oviposition did not result in more offspring in the 8 hours following mating, suggesting that mating with high sperm-viability genotypes leads to egg wastage for females shortly after copulation. Although mating with high sperm-viability males resulted in higher female fitness in the long term, high quality ejaculates would result in a short-term female fitness penalty, or at least lower realised fitness, potentially generating sexual conflict over optimal sperm viability.</p>

Data from: Feed-backs among inbreeding, inbreeding depression in sperm traits and sperm competition can drive evolution of costly polyandry

Ongoing ambitions are to understand the evolution of costly polyandry and its consequences for species ecology and evolution. Emerging patterns could stem from feed-back dynamics between the evolving mating system and its genetic environment, defined by interactions among kin including inbreeding. However, such feed-backs are rarely considered in non-selfing systems. We use a genetically-explicit model to demonstrate a mechanism by which inbreeding depression can select for polyandry to mitigate the negative consequences of mating with inbred males rather than avoiding inbreeding. Specifically, given inbreeding depression in sperm traits, costly polyandry evolved to ensure female fertility, without requiring explicit inbreeding avoidance. We show the mechanisms behind two main feed-backs. First, resulting sperm competition caused evolution of sperm traits and further mitigated the negative effect of inbreeding depression on female fertility. Second, the evolving mating system fed back to decrease population-wide homozygosity, and hence inbreeding. However, net overall reduction was small due to compound effects on the variances in sex-specific reproductive success and paternity skew. Purging of deleterious mutations did not eliminate inbreeding depression in sperm traits and hence selection for polyandry. Polyandry evolution, both directly and through sperm competition, might consequently facilitate evolutionary rescue for populations experiencing sudden increases in inbreeding.

Data from: A competitive environment influences sperm production, but not testes tissue composition, in house mice

Due to the physiological cost of sperm production, males are expected to be prudent in their expenditure and adjust their investment according to current social conditions. Strategic adjustments in sperm expenditure during development can be made via changes in testes size, sperm production rates, or testes tissue composition. Here, using house mice, we test the hypothesis that elevated sperm production is driven by a plastic response in the spatial organisation of the testes. We reared males under different social conditions (competitive vs. non-competitive) and quantified sperm number and the proportion of sperm‐producing tissue within the testes. Further, because sperm quality is a critical determinant of competitive fertilization success, we used computer-assisted sperm analysis to quantify six sperm motility traits. Our investigation revealed that males reared in an environment with a perceived risk of reproductive competition produced more sperm in the absence of changes in testes morphology. We discuss this result in relation to fixed and flexible phenotypically plastic responses to future competitive conditions, and conclude that adaptive adjustments in sperm number in response to the social environment are likely attributable to variation in sperm production rate. Further, we found no difference in in vitro sperm motility parameters among males from the different social environment regimes. Overall, this investigation improves our understanding of the mechanisms of male plastic responses to reproductive competition experienced during sexual development.

Data from: Paternity analysis of wild-caught females shows that sperm package size and placement influence fertilization success in the bushcricket Pholidoptera griseoaptera

In species where females store sperm, males may try to influence paternity by the strategic placement of sperm within the female's sperm storage organ. Sperm may be mixed or layered in storage organs, and this can influence sperm use beyond a 'fair raffle'. In some insects, sperm from different matings is packaged into discrete packets (spermatodoses), which retain their integrity in the female's sperm storage organ (spermatheca), but little is known about how these may influence patterns of sperm use under natural mating conditions in wild populations. We examined the effect of the size and position of spermatodoses within the spermatheca and number of competing ejaculates on sperm use in female dark bushcrickets (Pholidoptera griseoaptera) that had mated under unmanipulated field conditions. Females were collected near the end of the mating season, and seven hypervariable microsatellite loci were used to assign paternity of eggs laid in the laboratory. Females contained a median of three spermatodoses (range 1–6), and only six of the 36 females contained more than one spermatodose of the same genotype. Both the size and relative placement of the spermatodoses within the spermatheca had a significant effect on paternity, with a bias against smaller spermatodoses and those further from the single entrance/exit of the spermatheca. A higher number of competing males reduced the chances of siring offspring for each male. Hence, both spermatodose size and relative placement in the spermatheca influence paternity success.

opencc-zeroDec 2015View details →

Data from: Impaired sperm quality, delayed mating but no costs for offspring fitness in crickets winning a fight

The outcome of male-male contest competition is known to affect male mating success and is believed to confer fitness benefits to females through preference for dominant males. However, by mating with contest winners, females can incur significant costs spanning from decreased fecundity to negative effects on offspring. Hence identifying costs and benefits of male dominance on female fitness is crucial to unravel the potential for a conflict of interests between the sexes. Here we investigated males' pre- and post-copulatory reproductive investment and its effect on female fitness after a single contest a using the field cricket Gryllus bimaculatus. We allowed males to fight, and immediately measured their mating behaviour, sperm quality, and offspring viability. We found that males experiencing a fight, independently of the outcome, delayed matings but their courtship effort was not affected. However, winners produced sperm of lower quality (viability) compared to losers and to males that did not experience fighting. Results suggest a trade-off in resource allocation between pre- and post-mating episodes of sexual selection. Despite lower ejaculate quality we found no fitness costs (fecundity and viability of offspring) for females mated to winners. Overall our findings highlight the importance of considering fighting ability when assessing male reproductive success, as winners may be impaired in their competitiveness at a post-mating level.

Data from: Modeling strategic sperm allocation: tailoring the predictions to the species

Two major challenges exist when empirically testing the predictions of sperm allocation theory. First, the study species must adhere to the assumptions of the model being tested. Unfortunately, the common assumption of sperm allocation models that females mate a maximum of once or twice does not hold for many, if not most, multiply and sequentially mating animals. Second, a model's parameters, which dictate its predictions, must be measured in the study species. Common examples of such parameters, female mating frequency and sperm precedence patterns, are unknown for many species used in empirical tests. Here, we present a broadly applicable model, appropriate for multiply, sequentially mating animals, and test it in three species for which data on all the relevant parameter values are available. The model predicts that relative allocation to virgin females, compared to non-virgins, depends on the interaction between female mating rate and the sperm precedence pattern: relative allocation to virgins increases with female mating rate under first-male precedence, while the opposite is true under later-male precedence. Our model is moderately successful in predicting actual allocation patterns in the three species, including a cricket in which we measured the parameter values and performed an empirical test of allocation.

Data from: Female crickets assess relatedness during mate guarding and bias storage of sperm toward unrelated males

Recent evidence shows that females exert a post-copulatory fertilization bias in favour of unrelated males to avoid the genetic incompatibilities derived from inbreeding. One of the mechanisms suggested for fertilization biases in insects is female control over transport of sperm to the sperm-storage organs. We investigated post-copulatory inbreeding-avoidance mechanisms in females of the cricket Teleogryllus oceanicus. We assessed the relative contribution of related and unrelated males to the sperm stores of double-mated females. To demonstrate unequivocally that biased sperm storage results from female control rather than cryptic male choice, we manipulated the relatedness of mated males and of males performing post-copulatory mate guarding. Our results show that when guarded by a related male, females store less sperm from their actual mate, irrespective of the relatedness of the mating male. Our data support the notion that inhibition of sperm storage by female crickets can act as a form of cryptic female choice to avoid the severe negative effects of inbreeding.

Data from: Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect

Climate change is affecting biodiversity, but proximate drivers remain poorly understood. Here, we examine how experimental heatwaves impact on reproduction in an insect system. Male sensitivity to heat is recognised in endotherms, but ectotherms have received limited attention, despite comprising most of biodiversity and being more influenced by temperature variation. Using a flour beetle model system, we find that heatwave conditions (5 to 7 °C above optimum for 5 days) damaged male, but not female, reproduction. Heatwaves reduce male fertility and sperm competitiveness, and successive heatwaves almost sterilise males. Heatwaves reduce sperm production, viability, and migration through the female. Inseminated sperm in female storage are also damaged by heatwaves. Finally, we discover transgenerational impacts, with reduced reproductive potential and lifespan of offspring when fathered by males, or sperm, that had experienced heatwaves. This male reproductive damage under heatwave conditions provides one potential driver behind biodiversity declines and contractions through global warming.

Data from: Sperm competitive ability evolves in response to experimental alteration of operational sex ratio

In naturally polygamous organisms such as Drosophila, sperm competitive ability is one of the most important components of male fitness and is expected to evolve in response to varying degrees of male–male competition. Several studies have documented the existence of ample genetic variation in sperm competitive ability of males. However, many experimental evolution studies have found sperm competitive ability to be unresponsive to selection. Even direct selection for increased sperm competitive ability has failed to yield any measurable changes. Here we report the evolution of sperm competitive ability (sperm defense-P1, offense-P2) in a set of replicate populations of Drosophila melanogaster subjected to altered levels of male–male competition (generated by varying the operational sex ratio) for 55–60 generations. Males from populations with female-biased operational sex ratio evolved reduced P1 and P2, without any measurable change in the male reproductive behavior. Males in the male-biased regime evolved increased P1, but there was no significant change in P2. Increase in P1 was associated with an increase in copulation duration, possibly indicating greater ejaculate investment by these males. This study is one of the few to provide empirical evidence for the evolution of sperm competitive ability of males under different levels of male–male competition.

opencc-zeroDec 2015View details →

Data from: Post-copulatory opportunities for sperm competition and cryptic female choice provide no offspring fitness benefits in externally fertilizing salmon

There is increasing evidence that females can somehow improve their offspring fitness by mating with multiple males, but we understand little about the exact stage(s) at which such benefits are gained. Here, we measure whether offspring fitness is influenced by mechanisms operating solely between sperm and egg. Using externally fertilizing and polyandrous Atlantic salmon (Salmo salar), we employed split-clutch and split-ejaculate in vitro fertilization experiments to generate offspring using designs that either denied or applied opportunities for sperm competition and cryptic female choice. Following fertilizations, we measured 140 days of offspring fitness after hatch, through growth and survival in hatchery and near-natural conditions. Despite an average composite mortality of 61%, offspring fitness at every life stage was near-identical between groups fertilized under the absence versus presence of opportunities for sperm competition and cryptic female choice. Of the 21 551 and 21 771 eggs from 24 females fertilized under monandrous versus polyandrous conditions, 68% versus 67.8% survived to the 100-day juvenile stage; sub-samples showed similar hatching success (73.1% versus 74.3%), had similar survival over 40 days in near-natural streams (57.3% versus 56.2%) and grew at similar rates throughout. We therefore found no evidence that gamete-specific interactions allow offspring fitness benefits when polyandrous fertilization conditions provide opportunities for sperm competition and cryptic female choice.

opencc-zeroDec 2015View details →

Data from: Unravelling anisogamy: egg size and ejaculate size mediate selection on morphology in free-swimming sperm

Gamete dimorphism (anisogamy) defines the sexes in most multicellular organisms. Theoretical explanations for its maintenance usually emphasize the size-related selection pressures of sperm competition and zygote survival, assuming that fertilization of all eggs precludes selection for phenotypes that enhance fertility. In external fertilizers, however, fertilization is often incomplete due to sperm limitation, and the risk of polyspermy weakens the advantage of high sperm numbers that is predicted to limit sperm size, allowing alternative selection pressures to target free-swimming sperm. We asked whether egg size and ejaculate size mediate selection on the free-swimming sperm of Galeolaria caespitosa, a marine tubeworm with external fertilization, by comparing relationships between sperm morphology and male fertility across manipulations of egg size and sperm density. Our results suggest that selection pressures exerted by these factors may aid the maintenance of anisogamy in external fertilizers by limiting the adaptive value of larger sperm in the absence of competition. In doing so, our study offers a more complete explanation for the stability of anisogamy across the range of sperm environments typical of this mating system and identifies new potential for the sexes to coevolve via mutual selection pressures exerted by gametes at fertilization.

Data from: Ejaculate evolution in external fertilizers: influenced by sperm competition or sperm limitation?

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.

Data from: Sperm blocking is not a male adaptation to sperm competition in a parasitoid wasp

The extent to which sperm or ejaculate-derived products from different males interact during sperm competition – from kamikaze sperm to sperm incapacitation – remains controversial. Repeated matings in the parasitoid wasp Nasonia vitripennis lead to a short-term reduction of efficient sperm use by females, which is crucial for a haplodiploid organism when needing to allocate sex adaptively (i.e. by fertilizing eggs to produce daughters). Repeated matings by females in this species therefore constrain sex allocation through this "sperm-blocking" effect, eliciting a cost to polyandry. Here we explore the causes and consequences of sperm-blocking, and test the hypothesis that it is an ejaculate-related trait associated with sperm competition. First, we show that sperm blocking, which leads to an over-production of sons, is not correlated with success in either offensive or defensive roles in sperm competition. Then, we show that the extent of sperm blocking is not affected by self-self or kin-kin ejaculate interactions when compared to self vs non-self or kin versus non-kin sperm competition. Our results suggest that sperm blocking is not a sperm competition adaptation, but is instead associated with the mechanics of processing sperm in this species, which are likely shaped by selection on female reproductive morphology for adaptive sex allocation.