High Levels Of Sperm Competition Research Articles

Convergent rates of protein evolution identify novel targets of sexual selection in primates.

Sexual selection is the differential reproductive success of individuals, resulting from competition for mates, mate choice, or success in fertilization. In primates, this selective pressure often leads to the development of exaggerated traits which play a role in sexual competition and successful reproduction. In order to gain insight into the mechanisms driving the development of sexually selected traits, we used an unbiased genome-wide approach across 21 primate species to correlate individual rates of protein evolution to relative testes size and sexual dimorphism in body size, 2 anatomical hallmarks of sexual selection in mammals. Among species with presumed high levels of sperm competition, we detected strong conservation of testes-specific proteins responsible for spermatogenesis and ciliary form and function. In contrast, we identified accelerated evolution of female reproductive proteins expressed in the vagina, cervix, and fallopian tubes in these same species. Additionally, we found accelerated protein evolution in lymphoid tissue, indicating that adaptive immune functions may also be influenced by sexual selection. This study demonstrates the distinct complexity of sexual selection in primates revealing contrasting patterns of protein evolution between male and female reproductive tissues.

Fertilization modes and the evolution of sperm characteristics in marine fishes: Paired comparisons of externally and internally fertilizing species.

Fertilization mode may affect sperm characteristics, such as morphology, velocity, and motility. However, there is little information on how fertilization mode affects sperm evolution because several factors (e.g., sperm competition) are intricately intertwined when phylogenetically distant species are compared. Here, we investigated sperm characteristics by comparing seven externally and four internally fertilizing marine fishes from three different groups containing close relatives, considering sperm competition levels. The sperm head was significantly slenderer in internal fertilizers than in external fertilizers, suggesting that a slender head is advantageous for swimming in viscous ovarian fluid or in narrow spaces of the ovary. In addition, sperm motility differed between external and internal fertilizers; sperm of external fertilizers were only motile in seawater, whereas sperm of internal fertilizers were only motile in an isotonic solution. These results suggest that sperm motility was adapted according to fertilization mode. By contrast, total sperm length and sperm velocity were not associated with fertilization mode, perhaps because of the different levels of sperm competition. Relative testis mass (an index of sperm competition level) was positively correlated with sperm velocity and negatively correlated with the ratio of sperm head length to total sperm length. These findings suggest that species with higher levels of sperm competition have faster sperm with longer flagella relative to the head length. These results contradict the previous assumption that the evolution of internal fertilization increases the total sperm length. In addition, copulatory behavior with internal insemination may involve a large genital morphology, but this is not essential in fish, suggesting the existence of various sperm transfer methods. Although the power of our analyses is not strong because of the limited number of species, we propose a new scenario of sperm evolution in which internal fertilization would increase sperm head length, but not total sperm length, and change sperm motility.

Comparison of Prostate‐Specific Transglutaminase Function in the Great Apes

The copulatory plug is a hardened structure formed through semen coagulation post‐ejaculation which is theorized to protect against remating, stimulate the female reproductive tract, and aid in sperm release and transport. This structure is prevalent in species that experience high levels of sperm competition including chimpanzees and several other primates. Chimpanzees experience high levels of sperm competition due to their polygynandrous mating system. In polygynandry females will mate with multiple partners during an estrus cycle leading to direct competition between the sperm of each male to fertilize the same egg. This varies distinctly from polygynous and monogamous species, such as humans, where females mate with only one male and sperm competition is diminished. Based on previous work in rats, prostate‐specific transglutaminase 4 (TGM4) is implicated as the driving force of the formation of the copulatory plug. TGM4 is a member of the transglutaminase family of enzymes which catalyze the calcium‐dependent formation of an isopeptide bond between glutamine and lysine residues. While humans do not experience a great deal of sperm competition or form a copulatory plug, human semen goes through a similar process of post‐ejaculatory coagulation which is predicted to be carried out by TGM4 under the same mechanism. Interestingly, there are only seven amino acid differences between the human and chimpanzee TGM4s and yet the degree of coagulation between the two species is vastly different. The aim of this study to characterize and compare the function of these proteins to determine the major contributing factor in semen coagulation. The primary hypothesis was that chimpanzee TGM4 would have higher enzymatic activity and more readily cross‐link artificial substrates than human TGM4. To test this hypothesis, the coding sequences were acquired for human and chimpanzee TGM4 as well as eight other primate species. Using a maximum likelihood‐based method, we generated a gene tree of primate TGM4 and calculated dN/dS ratios for each branch. Human TGM4 had a dN/dS ratio of 1.04 suggesting neutral evolution while chimpanzee TGM4 had a ratio of >1 suggesting strong positive selection. We further predicted the sequence of TGM4 of the last human‐chimp ancestor using ancestral sequence reconstruction which utilizes the known phylogenetic tree and a maximum likelihood approach with the software package Phylogenetic Analysis by Maximum Likelihood (PAML). Coding sequences representing TGM4 from humans, chimpanzees, and the last human‐chimp ancestor were cloned into a mammalian expression vector containing a C‐terminal His6tag and were transfected into HEK‐293T cells. Purified TGM4 was used in an in‐vitro colorimetric enzymatic assay to quantify enzymatic activity. Our results suggest that mating system variation has led to differences in both sequence and function of seminal proteins. These functional differences speak to the impact of even a small number of mutations on protein function as well as the influence of environmental pressures on protein evolution.

Energy Metabolism and Hyperactivation of Spermatozoa from Three Mouse Species under Capacitating Conditions.

Mammalian sperm differ widely in sperm morphology, and several explanations have been presented to account for this diversity. Less is known about variation in sperm physiology and cellular processes that can give sperm cells an advantage when competing to fertilize oocytes. Capacitation of spermatozoa, a process essential for mammalian fertilization, correlates with changes in motility that result in a characteristic swimming pattern known as hyperactivation. Previous studies revealed that sperm motility and velocity depend on the amount of ATP available and, therefore, changes in sperm movement occurring during capacitation and hyperactivation may involve changes in sperm bioenergetics. Here, we examine differences in ATP levels of sperm from three mouse species (genus Mus), differing in sperm competition levels, incubated under non-capacitating and capacitating conditions, to analyse relationships between energetics, capacitation, and swimming patterns. We found that, in general terms, the amount of sperm ATP decreased more rapidly under capacitating conditions. This descent was related to the development of a hyperactivated pattern of movement in two species (M. musculus and M. spicilegus) but not in the other (M. spretus), suggesting that, in the latter, temporal dynamics and energetic demands of capacitation and hyperactivation may be decoupled or that the hyperactivation pattern differs. The decrease in ATP levels during capacitation was steeper in species with higher levels of sperm competition than in those with lower levels. Our results suggest that, during capacitation, sperm consume more ATP than under non-capacitating conditions. This higher ATP consumption may be linked to higher velocity and lateral head displacement, which are associated with hyperactivated motility.

Quantifying the costs of pre- and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort.

Although it is widely stated that both mating behavior and sperm traits are energetically costly for males, we currently lack empirical estimates of the relative costs to males of pre‐ versus postcopulatory investments. Such estimates require the experimental separation of the act of mating from that of ejaculation, which is a nontrivial logistical challenge. Here, we overcome this challenge using a novel morphological manipulation (gonopodium tip ablation) in the eastern mosquitofish (Gambusia holbrooki) to tease apart investment in mating effort from that in sperm replenishment following ejaculation. We quantified the relative cumulative costs of investing in mating effort and ejaculation by comparing somatic traits and reproductive performance among three types of males: ablated males that could attempt to mate but not ejaculate; unablated males that could both mate and ejaculate; and control males that had no access to females. We show that, after eight weeks, mating investment significantly reduces both body growth and immunocompetence and results in a significant decline in mating effort. In contrast, cumulative investment into sperm replenishment following ejaculation has few detectable effects that are only apparent in smaller males. These minor costs occur despite the fact that G. holbrooki has very high levels of sperm competition and multiple mating by both sexes, which is usually associated with elevated levels of sperm production. Crucially, our study is the first, to our knowledge, to experimentally compare the relative costs of pre‐ and postcopulatory investment on components of male fitness in a vertebrate.

Males of a Neotropical spider adjust prey‐gift construction but not mate search in response to sperm competition

AbstractIn scramble competition mating systems, males do not guard females and females usually mate polyandrously, leading to high levels of sperm competition. Mathematical models predict that males facing sperm competition can either decrease or increase their reproductive effort. To test how male reproductive responses vary according to sperm competition risk, we ran two experiments using the polyandrous gift‐giving spiderParatrechalea ornata. First, we tested whether males prefer substrates containing silk of unmated females than substrates containing silk of once‐mated females, competitor males or without silk. Males spent more time on substrates containing silk of females but showed no preference for unmated females, which indicates that males may optimize mate search by prioritizing substrates containing cues of potential mating partners. The lack of preference for unmated females suggests that males cannot detect female mating status from silk or that the costs of searching preferentially for unmated females are high in the field. Second, we tested whether males adjust prey‐gift construction when facing sperm competition risk. Experimental groups (substrate containing silk of an unmated female and silk of another malevs. substrate containing only silk of an unmated female) did not differ in the frequency of gift construction, latency to gift construction and number of flies added to the gift. However, males facing sperm competition risk constructed gifts with less silk, suggesting the occurrence of a less evident form of male mate choice based on differential allocation of resources to prey‐gift. Additionally, given the trade‐off between investing in prey‐gifts quantity or quality, a lower silk investment should enable males to increase the number of gifts constructed and the number of courted females. Taken together, our results indicate that males detect female and male pheromones on substrate and adjust the construction of prey‐gifts in response to apparent sperm competition risk.

How sperm competition shapes the evolution of testes and sperm: a meta-analysis.

Females of many species mate with multiple males, thereby inciting competition among ejaculates from rival males for fertilization. In response to increasing sperm competition, males are predicted to enhance their investment in sperm production. This prediction is so widespread that testes size (correcting for body size) is commonly used as a proxy of sperm competition, even in the absence of any other information about a species' reproductive behaviour. By contrast, a debate about whether sperm competition selects for smaller or larger sperm has persisted for nearly three decades, with empirical studies demonstrating every possible response. Here, we synthesize nearly 40 years of sperm competition research in a meta-analytical framework to determine how the evolution of sperm number (i.e. testes size) and sperm size (i.e. sperm head, midpiece, flagellum and total length) is influenced by varying levels of sperm competition across species. Our findings support the long-held assumption that higher levels of sperm competition are associated with relatively larger testes. We also find clear evidence that sperm competition is associated with increases in all components of sperm length. We discuss these results in the context of different theoretical predictions and general patterns in the breeding biology and selective environment of sperm. This article is part of the theme issue 'Fifty years of sperm competition'.

The development, evaluation, and illustration of a timeline procedure for testing the role of sperm competition in the evolution of sexual traits using paternity data

The empirical study of the role of sperm competition in the evolution of sexual traits has historically been problematic through the inability either to measure sperm competition levels directly in the present or to reconstruct changes in the evolutionary past. Here, we develop and test a procedure based on paternity data that potentially permits both. For our pilot study, we use the rate of change of the seminal protein gene SEMG2 for catarrhine primates published by Dorus et al. (Nat Genet 36:1326–1329, 2004). From their data, Dorus et al. proposed a two-part hypothesis: (1) sperm competition plays a role in the evolution of the SEMG2 gene and (2) higher levels of sperm competition generate more positive selection for change in SEMG2 than lower levels. Dorus et al. were limited, however, by being able to use only proxy measures of sperm competition and only seven “recent” segments of catarrhine primate phylogeny. Here, we develop a “timeline procedure” that permits the Dorus hypothesis to be tested using data from across the whole of catarrhine phylogeny. Our analysis supports part (1) of the Dorus hypothesis but questions part (2), suggesting instead that changes in level of sperm competition have a more powerful influence on the rate of evolution of traits than the level of sperm competition itself. We conclude that the timeline procedure developed here could be a valuable investigative tool in the role of sperm competition in the evolution of sexual traits measured over evolutionary time such as SEMG2. The empirical study of the role of sperm competition in the evolution of sexual traits has historically been problematic through the inability to measure sperm competition levels directly in the present and to reconstruct changes in the evolutionary past. Here, we test a “timeline procedure” based on paternity data that potentially permits both. For our pilot study, we use the rate of change of the seminal protein gene SEMG2 for catarrhine primates published by Dorus et al. (Nat Genet 36:1326–1329, 2004). Whereas Dorus et al. were limited to using proxy measures for only “recent” segments of catarrhine primate phylogeny, our method permits direct measures of sperm competition to be applied across the whole of Catarrhine phylogeny. We conclude that this new procedure could be valuable for investigation of the role of sperm competition in the evolution of a wide range of sexual traits.

Dunnock social status correlates with sperm speed, but fast sperm does not always equal high fitness.

Sperm competition theory predicts that males should modulate sperm investment according to their social status. Sperm speed, one proxy of sperm quality, also influences the outcome of sperm competition because fast sperm cells may fertilize eggs before slow sperm cells. We evaluated whether the social status of males predicted their sperm speed in a wild population of dunnocks (Prunella modularis). In addition to the traditional analysis of the average speed of sperm cells per sample, we also analysed subsamples of the fastest sperm cells per sample. In other words, we systematically evaluated the effects of including different numbers of the fastest sperm in our analyses, ranging from the 5-fastest sperm cells to the 100-fastest sperm cells in a sample. We further evaluated whether fitness, defined here as the number of chicks sired per male per breeding season, relates to the sperm speed in the same population. We found that males in monogamous pairings (i.e. low levels of sperm competition), produced the slowest sperm cells, whereas subordinate males in polyandrous male-male coalitions (i.e. high levels of sperm competition) produced the fastest sperm cells. This result was consistent regardless of the number of fastest sperm included in our analyses, but statistical support was conditional on the number of sperm cells included in the analysis. Interestingly, we found no significant relationship between fitness and sperm speed, which suggests that it is possible that the differential mating opportunities across social status levelled out any possible difference. Our study also suggests that it is important to identify biologically meaningful subsets of fastest sperm and cut-offs for inclusions for assessing sperm competition via sperm speed.

A phylogenetic comparative analysis on the evolution of sequential hermaphroditism in seabreams (Teleostei: Sparidae)

The Sparids are an ideal group of fishes in which to study the evolution of sexual systems since they exhibit a great sexual diversity, from gonochorism (separate sexes) to protandrous (male-first) and protogynous (female-first) sequential hermaphroditism (sex change). According to the size-advantage model (SAM), selection should favour sex change when the second sex achieves greater reproductive success at a larger body size than the first sex. Using phylogenetic comparative methods and a sample of 68 sparid species, we show that protogyny and protandry evolve from gonochorism but evolutionary transitions between these two forms of sequential hermaphroditism are unlikely to happen. Using male gonadosomatic index (GSI) as a measure of investment in gametes and proxy for sperm competition, we find that, while gonochoristic and protogynous species support the predictions of SAM, protandrous species do not, as they exhibit higher GSI values than expected even after considering mating systems and spawning modes. We suggest that small males of protandrous species have to invest disproportionally more in sperm production than predicted not only when spawning in aggregations, with high levels of sperm competition, but also when spawning in pairs due to the need to fertilize highly fecund females, much larger than themselves. We propose that this compensatory mechanism, together with Bateman’s principles in sequential hermaphrodites, should be formally incorporated in the SAM.

Asymmetries in reproductive anatomy: insights from promiscuous songbirds

Abstract Directional asymmetry in gonad size is commonly observed in vertebrates and is particularly pronounced in birds, where the left testis is frequently larger than the right. The adaptive significance of directional asymmetry in testis size is poorly understood, and whether it extends beyond the testes (i.e. side-correspondent asymmetry along the reproductive tract) has rarely been considered. Using the Maluridae, a songbird family exhibiting variation in levels of sperm competition and directional testis asymmetry, yet similar in ecology and life history, we investigated the relative roles of side-correspondence and sperm competition on male reproductive tract asymmetry at both inter- and intraspecific levels. We found some evidence for side-correspondent asymmetry. Additionally, sperm competition influenced directional asymmetry at each end of the reproductive tract: species experiencing higher levels of sperm competition had a relatively larger right testis and relatively more sperm in the right seminal glomerus. Within red-backed fairy-wrens (Malurus melanocephalus), auxiliary males had relatively more sperm in the left seminal glomerus, in contrast to a right-bias asymmetry throughout the reproductive tract in breeding males. Given that the number of sperm is important for competitive fertilization success, our results suggest that sperm competition shapes reproductive asymmetries beyond testis size, with likely functional consequences for male reproductive success.

The bold and the sperm: positive association between boldness and sperm number in the guppy.

Assessing the consequences of personality traits on reproductive success is one of the most important challenges in personality studies and critical to understand the evolutionary implications of behavioural variability among animals. Personality traits are typically associated with mating acquisition in males, and, hence, linked to variation in their reproductive success. However, in most species, sexual selection continues after mating, and sperm traits (such as sperm number and quality) become very important in determining post-mating competitive success. Here, we investigate whether variation in personality traits is associated with variation in sperm traits using the guppy (Poecilia reticulata), a species with high levels of sperm competition. We found a positive association between boldness and sperm number but not sperm velocity, suggesting that bolder males have increased post-copulatory success than shyer individuals. No association was found between exploration and sperm traits. Our work highlights the importance of considering post-copulatory traits when investigating fitness consequences of personality traits, especially in species with high levels of female multiple matings and hence sperm competition.

Positive correlations between pre‐ and post‐copulatory sexual traits in warblers

Theoretical models predict that investment in pre‐copulatory and post‐copulatory sexually selected traits should trade‐off. At the macroevolutionary scale, the majority of studies to date have focused on male weaponry as the target of pre‐copulatory sexual selection, but the trade‐off should equally apply to traits used to attract females, such as bird song and plumage. We studied the Old World leaf warblers (Phylloscopidae), a group of socially monogamous songbirds that experience relatively high levels of sperm competition. We examined the relationships between song duration and number of elements in the song with sperm length across 21 species, and between the same song variables and combined testes mass in a subset of these species (n = 10). Across species, these song variables and testes mass/sperm length were generally positively correlated, albeit not statistically significantly so or with borderline significance. In contrast to theory, we found no evidence for negative associations between pre‐ and post‐copulatory traits. We argue that this is a consequence of males of some species investing more into overall fertilization success (i.e. the sum of pre‐ and post‐copulatory sexual selection) than males of other species, and high fertilization success is achieved through investment into both mate attraction and sperm competition.

Is male reproductive senescence minimized in Mus species with high levels of sperm competition?

This work was supported by a Ramon y Cajal fellowship from the Spanish Ministry of Economy and Competitiveness (RYC-2011-07943) and a Marie Curie Career Integration Grant (PCIG11-GA-2012-321888) to J.d.-T., a Juan de la Cierva fellowship from the Spanish Ministry of Economy and Competitiveness to M.T. (JCI-2011-10381) and grants from the Spanish Ministry of Economy and Competitiveness (CGL2011-26341 and CGL2016-80577-P to E.R.S.R. and CGL2012-37423 to J.d.-T.).

High level of sperm competition may increase transfer of accessory gland products carried by the love dart of land snails.

Postcopulatory adaptations that increase reproductive success compared to rivals, like the transfer of accessory gland products that promote paternity, are common when sperm competition occurs among males. In land snails, the dart shooting behavior and its adaptive significance, in promoting individual fitness through enhanced paternity of the successful dart shooter, have been considered such an adaptation. The fitness result gained is mediated by the transfer of mucus components on the love dart capable of altering the physiology of the receiver's reproductive tract. In this context, dart shooting and mucus transfer could be considered as processes targeted by sexual selection. While the effect of dart mucus is beneficial for the dart user, so far it has remained unknown whether its transport is greater when snails experience a higher level of sperm competition. Here, we report results of a study on inter‐ and intraspecific variations of dart and mucus gland morphometry, considered to be traits reflecting the ability of snails to adjust the production and transfer of mucus under varying sperm competition scenarios. We investigated four populations with different densities from four dart‐bearing species, Arianta arbustorum, Cepaea nemoralis, Cornu aspersum, and Helix lucorum. The results indicate that different adaptations of these traits occur among the studied species that all seem to achieve the same goal of transferring more mucus when sperm competition is higher. For example, the presence of longer and more branched mucous glands or an increase in dart surface most likely reflect increased mucus production and enhanced ability of mucus transport, respectively. Interestingly, the species for which the use of the dart is reported to be facultative, A. arbustorum, did not show any variation among the examined traits. To conclude, sexual selection in the form of sperm competition intensity seems to be an important selective force for these simultaneously hermaphroditic dart‐bearing snails, driving differences in sexual traits.

No evidence for parental age effects on offspring leukocyte telomere length in free-living Soay sheep

In humans, the effect of paternal age at conception (PAC) on offspring leukocyte telomere length (LTL) is well established, with older fathers thought to pass on longer telomeres to their offspring in their sperm. Few studies have looked for PAC effects in other species, but it has been hypothesised that the effect will be exacerbated in polygamous species with higher levels of sperm competition and production. We test for maternal (MAC) and paternal age at conception effects on offspring LTL in Soay sheep, a primitive breed experiencing strong sperm competition. We use qPCR to measure relative telomere length in 389 blood samples (n = 318 individuals) collected from an unmanaged population of sheep on St Kilda, where individual age and parentage are known. We find no evidence that either MAC or PAC are associated with LTL in offspring across the age range, or when considering only young lambs (n = 164). This is the first study to test for parental age effects on offspring LTL in a wild mammal population, and the results contrast with the findings of numerous human studies that find a PAC effect, as well as predictions of a stronger PAC effect in polygamous species.

Species-level divergences in multiple functional traits between the two endemic subspecies of Blue Chaffinches Fringilla teydea in Canary Islands

One of the biggest challenges in avian taxonomy is the delimitation of allopatric species because their reproductive incompatibility cannot be directly studied in the wild. Instead, reproductive incompatibility has to be inferred from multiple, divergent character sets that indicate a low likelihood of allopatric populations amalgamating upon secondary contact. A set of quantitative criteria for species delimitation has been developed for avian taxonomy. Here, we report a broad multi-trait comparison of the two insular subspecies of the Blue Chaffinch Fringilla teydea, endemic to the pine forests of Tenerife (ssp. teydea) and Gran Canaria (ssp. polatzeki) in the Canary Islands. We found that the two taxa were reciprocally monophyletic in their whole mitogenomes and two Z chromosome introns. The genetic distance in mitogenomes indicates around 1 Mya of allopatric evolution. There were diagnostic differences in body morphometrics, song and plumage reflectance spectra, whose combined divergence score (=11) exceeds the threshold level (=7) set for species delimitation by Tobias et al. (Ibis 152:724–746, 2010). Moreover, we found a marked divergence in sperm lengths with little range overlap. Relatively long sperm with low intra- and intermale CV compared to other passerines suggest a mating system with high levels of sperm competition (extrapair paternity) in these taxa. The large and diagnostic divergences in multiple functional traits qualify for species rank, i.e., Tenerife Blue Chaffinch (Fringilla teydea) and Gran Canaria Blue Chaffinch (Fringilla polatzeki). We encourage a wider use of sperm traits in avian taxonomy because sperm divergences might signal reproductive incompatibility at the postcopulatory prezygotic stage, especially in species with sperm competition.

A cost for high levels of sperm competition in rodents: increased sperm DNA fragmentation.

Sperm competition, a prevalent evolutionary process in which the spermatozoa of two or more males compete for the fertilization of the same ovum, leads to morphological and physiological adaptations, including increases in energetic metabolism that may serve to propel sperm faster but that may have negative effects on DNA integrity. Sperm DNA damage is associated with reduced rates of fertilization, embryo and fetal loss, offspring mortality, and mutations leading to genetic disease. We tested whether high levels of sperm competition affect sperm DNA integrity. We evaluated sperm DNA integrity in 18 species of rodents that differ in their levels of sperm competition using the sperm chromatin structure assay. DNA integrity was assessed upon sperm collection, in response to incubation under capacitating or non-capacitating conditions, and after exposure to physical and chemical stressors. Sperm DNA was very resistant to physical and chemical stressors, whereas incubation in non-capacitating and capacitating conditions resulted in only a small increase in sperm DNA damage. Importantly, levels of sperm competition were positively associated with sperm DNA fragmentation across rodent species. This is the first evidence showing that high levels of sperm competition lead to an important cost in the form of increased sperm DNA damage.

Sperm competition-induced plasticity in the speed of spermatogenesis.

BackgroundSperm competition between rival ejaculates over the fertilization of ova typically selects for the production of large numbers of sperm. An obvious way to increase sperm production is to increase testis size, and most empirical work has focussed on this parameter. Adaptive plasticity in sperm production rate could also arise due to variation in the speed with which each spermatozoon is produced, but whether animals can respond to relevant environmental conditions by modulating the kinetics of spermatogenesis in this way has not been experimentally investigated.ResultsHere we demonstrate that the simultaneously hermaphroditic flatworm Macrostomum lignano exhibits substantial plasticity in the speed of spermatogenesis, depending on the social context: worms raised under higher levels of sperm competition produce sperm faster.ConclusionsOur findings overturn the prevailing view that the speed of spermatogenesis is a static property of a genotype, and demonstrate the profound impact that social environmental conditions can exert upon a key developmental process. We thus identify, to our knowledge, a novel mechanism through which sperm production rate is maximised under sperm competition.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0629-9) contains supplementary material, which is available to authorized users.

Direct reciprocity stabilizes simultaneous hermaphroditism at high mating rates: A model of sex allocation with egg trading.

Simultaneous hermaphroditism is predicted to be unstable at high mating rates given an associated increase in sperm competition. The existence of reciprocal egg trading, which requires both hermaphroditism and high mating rates to evolve, is consequently hard to explain. We show using mathematical models that the presence of a trading economy creates an additional fitness benefit to egg production, which selects for traders to bias their sex allocation toward the female function. This female-biased sex allocation prevents pure females from invading a trading population, thereby allowing simultaneous hermaphroditism to persist stably at much higher levels of sperm competition than would otherwise be expected. More generally, our model highlights that simultaneous hermaphroditism can persist stably when mating opportunities are abundant, as long as sperm competition remains low. It also predicts that reciprocity will select for heavier investment in the traded resource.