Academic literature on the topic 'Postcopulatory sexual selection'

The extreme morphological variability of the baculum across mammals is thought to be the result of sexual selection (particularly, high levels of postcopulatory selection). However, the evolutionary trajectory of the mammalian baculum is little studied and evidence for the adaptive function of the baculum has so far been elusive. Here, we use Markov chain Monte Carlo methods implemented in a Bayesian phylogenetic framework to reconstruct baculum evolution across the mammalian class and investigate the rate of baculum length evolution within the primate order. We then test the effects of testes mass (postcopulatory sexual selection), polygamy, seasonal breeding and intromission duration on the baculum in primates and carnivores. The ancestral mammal did not have a baculum, but both ancestral primates and carnivores did. No relationship was found between testes mass and baculum length in either primates or carnivores. Intromission duration correlated with baculum presence over the course of primate evolution, and prolonged intromission predicts significantly longer bacula in extant primates and carnivores. Both polygamous and seasonal breeding systems predict significantly longer bacula in primates. These results suggest the baculum plays an important role in facilitating reproductive strategies in populations with high levels of postcopulatory sexual selection.

Two decades ago, von Schantz et al . (von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H. 1999 Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. B 266, 1–12. ( doi:10.1098/rspb.1999.0597 )) united oxidative stress (OS) biology with sexual selection and life-history theory. This set the scene for analysis of how evolutionary trade-offs may be mediated by the increase in reactive molecules resulting from metabolic processes at reproduction. Despite 30 years of research on OS effects on infertility in humans, one research area that has been left behind in this integration of evolution and OS biology is postcopulatory sexual selection—this integration is long overdue. We review the basic mechanisms in OS biology, why mitochondria are the primary source of ROS and ATP production during oxidative metabolism, and why sperm, and its performance, is uniquely susceptible to OS. We also review how postcopulatory processes select for antioxidation in seminal fluids to counter OS and the implications of the net outcome of these processes on sperm damage, sperm storage, and female and oocyte manipulation of sperm metabolism and repair of DNA to enhance offspring fitness. This article is part of the theme issue ‘Fifty years of sperm competition’.

Sexual selection is a driving force in sexually reproducing organisms and strongly shapes their evolution. In the last three decades, sexual selection research has seen a rapid growth, and both theoretical and empirical work has clarified many components of pre- and postcopulatory sexual selection. Despite that, the coexistence of two basic observations still forms an unsolved evolutionary question: in natural populations genetic variation is found in almost all traits in the presence of strong natural and sexual selection. As selection should deplete variability those two observations are in direct conflict. This problem attracted the attention of many researchers, as it regards potentially most of the numerous traits describing an organism’s phenotype, or at least all the traits under some selection. During my PhD I explored part of this field of study, focusing on sexually selected male traits. Most of the efforts done to understand this evolutionary contradiction have been done in a precopulatory context, with particular attention to the prominent case of the so called ‘lek-paradox’. However, whenever females are sexually promiscuous, a directional selection for traits associated with sperm competition success is expected to arise. As ejaculate characteristics are expected, and actually known, to play a crucial role in determining the fitness outcome of males, selection acting on them should be strong and as a consequence their variability reduced. Yet, as for precopulatory traits, there are many experimental evidences that variability in postcopulatory traits is unexpectedly high. Many hypotheses have been formulated to explain the maintenance of genetic variability of sexually selected traits. During my PhD I tested some prediction of three main models applicable to both pre- and postcopulatory traits: first that selection constrains and non linear selection are acting on the set of traits defining the male phenotype. Second, I verified that resource trade-offs are present between pre- and postcopulatory traits, as proposed by Parker’s sperm competition theory. Third, I tested the fundamental assumption of the ‘genic capture hypothesis’ that sexually selected traits are condition dependent. I performed four main experiments using the guppy, Poecilia reticulata. This small tropical fresh-water fish is well suited for my purposes as traits subject to both pre- (male ornamentation, size, and behaviour) and postcopulatory selection (sperm number, velocity, and viability) exhibit high levels of phenotypic and additive genetic variation. With the first experiment (manuscript 1) I characterized, for the first time, the selection acting in a whole on both pre- and postcopulatory traits. I then measured the long term cost of sperm production (manuscript 2) with the aim of determine the trade-offs present between pre- and postcopulatory traits. With the last two experiments (manuscripts 3 and 4) I tested condition dependence of a wide set of sexually selected traits. My results suggest that in this species non linear selection may be more important than previously estimated and, in particular, that disruptive and correlational selection can contribute to maintain polymorphisms in sexually selected traits. Moreover investment in ejaculate is traded off with investment in obtaining mating, in agreement with sperm competition theory. Lastly, both pre- and postcopulatory sexually selected traits show a strong condition dependence, thus confirming one assumption of the ‘genic capture hypothesis’.
La selezione sessuale, descritta da Darwin nella sua opera “The Descent of Man and Selection in Relation to Sex”(1871) è una delle forze trainanti in natura e, nella maggior parte degli esseri viventi, determina fortemente la loro evoluzione. Negli ultimi tre decenni, la ricerca scientifica nell’ambito della selezione sessuale ha visto una rapida crescita, e numerosissimi lavori sia teorici che sperimentali hanno chiarito numerosi aspetti della selezione sessuale sia pre- che postcopulatoria. Nonostante ciò, la coesistenza di due fondamentali condizioni in natura fa si che esista ancora un paradosso evolutivo irrisolto: nella maggior parte dei caratteri si osserva una grande variabilità genetica nonostante la presenza di una forte selezione, sia naturale che sessuale. Poiché la selezione dovrebbe esaurire la variabilità genetica, queste due condizioni (variabilità da una parte e selezione dall’altra) sono in diretto conflitto. Poiché questa situazione riguarda la maggior parte dei tratti che formano il fenotipo di un organismo, o almeno tutti quei caratteri sotto una qualche forma di selezione, è facilmente immaginabile come questo problema abbia attirato l’attenzione di moltissimi ricercatori. Durante il mio dottorato di ricerca ho mi sono dedicato allo studio di una parte di questo problema, concentrandomi sui caratteri maschili selezionati sessualmente. Questo campo è stato ampliamente studiato ma la maggior parte degli sforzi fatti per comprendere questa contraddizione è stata compiuta esclusivamente in un contesto di selezione precopulatoria, ed in particolare per quanto riguarda un suo caso particolare, quello del paradosso del lek. Tuttavia, nel caso in cui le femmine di una specie siano sessualmente promiscue (situazione quasi totalmente diffusa nel regno animale), ci si aspetta la presenza di una selezione direzionale per i caratteri maschili legati alla competizione spermatica. Ed infatti quello che si osserva è che le caratteristiche dell’eiaculato hanno un ruolo importante nel determinare il successo riproduttivo maschile. La selezione su questi tratti è quindi forte ma, come per i caratteri precopulatori, numerose evidenze sperimentali dimostrano la presenza di un’elevata variabilità sia genetica che fenotipica in caratteri soggetti a selezione postcopulatoria. Molte ipotesi sono state formulate per spiegare il mantenimento della variabilità genetica nei tratti selezionati sessualmente. In particolare, durante il mio dottorato ho testato le previsioni di tre di queste principali teorie, applicabili sia ai tratti pre- che postcopulatori. Per prima cosa ho verificato la presenza di selezione non lineare disruptiva e correlazionale prendendo in considerazione un ampio set di caratteri maschili. In secondo luogo, ho verificato che esistano dei trade-off di tipo energetico tra i tratti pre- e postcopulatori, come proposto nella ‘teoria della competizione spermatica’ di Parker. Infine, ho testato una delle condizioni fondamentali della teoria della ‘cattura genica’ proposta da Rowe e Houle (1996) e cioè che i tratti selezionati sessualmente siano condizione-dipendenti. Durante il dottorato ho svolto quattro esperimenti principali utilizzando come specie modello Poecilia reticulata, comunemente chiamata guppy. Questo piccolo pesce tropicale d'acqua dolce è particolarmente adatto per i miei scopi. I maschi presentano infatti caratteristiche soggette sia a selezione precopulatoria (ornamenti, dimensioni e comportamento sessuale) che a selezione postcopulatoria (numero, velocità e vitalità degli spermatozoi) ed inoltre si osserva in questi caratteri un’elevata varianza genetica additiva. Appare quindi evidente la presenza della contraddizione prima descritta. Con il primo esperimento (primo articolo) ho descritto, per la prima volta, la selezione non lineare che agisce sull’insieme dei tratti sia pre- che postcopulatori. Ho poi misurato il costo a lungo termine imposto dalla produzione di spermi (secondo articolo) con l'obiettivo di determinare i trade-off presenti tra i tratti pre- e postcopulatori. Negli ultimi due articoli (terzo e quarto) ho testato l’ipotesi di condizione-dipendenza in un ampio set di tratti selezionati sessualmente. I miei risultati suggeriscono che in questa specie la selezione non lineare può essere più importante di quanto stimato in precedenza e, in particolare, che la selezione disruptiva e correlazionale possono contribuire a mantenere il polimorfismo osservato nei tratti selezionati sessualmente. Inoltre l’investimento a livello postcopulatorio nell’eiaculato presenta per i maschi di Poecilia un costo in termini di successo precopulatorio (possibilità di accoppiarsi), in accordo con la teoria della competizione spermatica. Infine, i tratti sessualmente selezionati, sia pre- che postcopulatori, mostrano una forte dipendenza dalla condizione del maschio, confermando così uno degli assunti dell’ ipotesi della cattura genica.

During the final stage of courtship, the garden snail Helix aspersa attempts to stab its mating partner with a mucus-coated calcareous "love dart." I present evidence supporting two predictions of the most promising hypothesis for the adaptive significance of this behavior: that the dart serves to increase the reproductive success of the shooter by increasing the numerical representation of its sperm in the recipient's storage organ (the sperm loading hypothesis). First, I demonstrate that once-mated snails store more of the sperm transferred by successful shooters than by unsuccessful shooters. Second, I demonstrate that this biased storage results in higher paternity scores for successful shooters relative to unsuccessful shooters in the clutches of multiply mated recipients. Moreover, I present evidence that body size and mating order influence the outcome of sperm competition in snails. Finally, I propose a novel mechanism to explain the observed pattern of sperm utilization in H. aspersa based on the motility of stored allosperm.

[Truncated abstract] Despite the costs associated with mating, females of many taxa solicit multiple mates during a single reproductive event (polyandry). Polyandry is clearly adaptive when females gain direct benefits from males at mating. However, polyandry has also been shown to increase female fitness in the absence of direct benefits. Thus, a number of genetic benefit hypotheses have been developed to account for the origin of this behaviour. Although not mutually exclusive, a distinction lays between genetic benefits that propose defense against reproductive failure (nonadditive genetic effects), and those that propose benefits from intrinsic sire effects (additive genetic effects). Nonadditive genetic benefits of polyandry have been documented in a number of species; by soliciting multiple mates females can avoid inbreeding and other forms of incompatibility between parental genotypes. Polyandry may also increase female reproductive success when genetically superior males have greater success in sperm competition, and produce better quality offspring. An inevitable consequence of polyandry is that sperm from rival males will overlap in the female reproductive tract and compete to fertilise the ova. The outcome of sperm competition is typically determined by bias in sperm use by the females, interactions between parental genotypes, and ejaculate characteristics that provide a fertilisation advantage. Thus, sperm competition is recognised as a persuasive force in the evolution of male reproductive traits. Comparative analyses across species, and competitive mating trials within species have suggested that sperm competition can influence the evolution of testis size and sperm production, and both sperm form and sperm function. ... After six generations of selection I observed phenotypic divergence in litter size - litter size increased in the polyandrous lines but not in the monandrous lines. This result was not attributable to inbreeding depression, or environmental/maternal effects associated with mating regime. Genetic benefits associated with polyandry could account for this result if increased litter size were attributable to increased embryo survival. However, males from the polyandrous lineages were subject to sperm competition, and evolved ejaculates with more sperm, suggesting that evolutionary increases in litter size may in part be due to improved male fertility. Finally, Chapter Five is an investigation of the natural variation in levels of polyandry in the wild, and the potential for sperm competition to drive macroevolutionary changes in male reproductive traits among geographically isolated island populations of house mice. I sampled seven island populations of house mice along the coast of Western Australia and, by genotyping pregnant females and their offspring, determined the frequency of multiply sired litters within each population. I applied the frequency of multiple paternity as an index of the risk of sperm competition, and looked for selective responses in testis size and ejaculate traits. I found that the risk of sperm competition predicted testis size across the seven island populations. However, variation in sperm traits was not explained by the risk of sperm competition. I discuss these results in relation to sperm competition theory, and extrinsic factors that influence ejaculate quality.

Given multiple matings from females, sexual selection continues after insemination in the form of postcopulatory sexual selection. This process is formed by two main mechanisms: sperm competition (competition of sperm of two or more males for the fertilization of the eggs of the same female) and cryptic female choice. These act as powerful selective pressures for the evolution of reproductive biology of both males and females. The aim of this thesis is to analyze the relative importance of sperm competition and cryptic female choice in determining a male reproductive success. The study species is the guppy (Poecilia reticulata), a freshwater fish, ovoviviparous with internal fertilization. Using artificial insemination, I studied if females can obtain fecundity benefits from mating with colourful males (as predicted by Sheldon's Phenotype-linked fertility hypothesis), the role of sperm number and sperm quality for sperm competition success, repeatability of a male's fertilization success and the role of MHC genes in non directional cryptic female choice. This technique allows to control for many potential confounding variables, as order of mating, number of sperm inseminated and cryptic female choice. From the experiments, it emerges that directional processes in this species are more important for fertilization success rather than non directional processes, even if a part of variance in fertilization success is explained by a male's similarity for MHC genotype with the female.

Postcopulatory sexual selection—sperm competition and cryptic female choice—has become a major area of research over the past 40 years. Within this field there are many outstanding questions at every level of analysis, from proximate to ultimate. The fitness consequences for both sexes in the period after copulation and before fertilization are considerable, but are obscured within the female reproductive tract. Our understanding of postcopulatory mechanisms is especially sparse in taxa other than birds and insects. Nearly nothing is known in reptiles except that multiple paternity is common and widespread, and often results from long-term sperm storage across breeding seasons. We present some of the very first data on the determinants of fertilization success in the context of sperm competition in reptiles, a group that accounts for 30% of terrestrial vertebrates. In the first chapter, "Asymmetric gametic isolation between two populations of red-sided garter snakes", we discuss the use of between-population crosses to reveal gametic isolation. The effect of population density and operational sex ratios on mating systems and the speciation process has fueled theoretical debate. We attempted to address these issues using two populations of red-sided garter snakes (Thamnophis sirtalis parietalis) from Manitoba, Canada. Our study populations differ markedly in their density mating aggregations, with a 10-fold difference between them. Using microsatellite markers for paternity analysis of litters produced from within and between population crosses. We found that the population with highest aggregation density, and presumably with the highest level of sexual conflict (i.e., when the evolutionary interests of the sexes differ) over mating, was also the population that exhibited homotypic sperm precedence. The less dense population showed a distinct postcopulatory male-size advantage. We also demonstrated that sperm stored within the female over hibernation can father 20-30% of offspring in a litter. In the second chapter, "Sperm competition and mate-order effects in red-sided garter snakes", we test whether females use mate-order effects to ensure that a larger (fitter) male will sire her offspring. Does that second male should have precedence in sperm competition? We tested for second-male precedence using singly-mated females that mated with a second male. Average proportion of paternity was shared equally among the first (P₁, i.e., proportion of offspring from a litter fathered by the first male to mate) and second males (P₂) to mate, and stored sperm (P[subscript ss]). This may be a case where last male precedence breaks down with more than two males. All females were spring virgins (they had not mated that spring, but may have stored sperm from fall matings); thus sperm stored presumably from fall matings is important in this system. As the interval between matings increased P₁ increased at the expense of P[subscript ss]. As the second male to mate's copulation duration increased, P₁ also increased at the expense of P₂. This last result may indicate female influence over sperm transfer during coerced matings. Copulatory plugs (CPs) are found in many taxa, but the functional significance is debated. Male garter snakes produce a gelatinous copulatory plug during mating that occludes the opening of the female reproductive tract for approximately two days. In chapter three, "Not just a chastity belt: the role of mating plugs in red-sided garter snakes revisited", we experimentally tested the role of the CPs. In snakes, sperm are produced in the testes and delivered through the ductus deferens, and the copulatory plug is thought to be produced by the sexual segment of the kidney and conveyed through the ureter. We manipulated the delivery of the two fluids separately by ligating the ducts. We confirmed that the CP is not formed in ureter-ligated males and that sperm leaks out immediately after copulation. The CP is analogous to a spermatophore. The protein matrix contains most of the sperm which are liberated as the plug dissolves within the female's vaginal pouch. One of the fundamental principles in sperm competition is that increased sperm numbers increase the odds of winning in competitions for fertilization success and males will adjust their ejaculate relative to competition and the quality of his mate. In chapter four, "Sperm depleted males and the unfortunate females who mate with them", we detect significant among-male variation in the number of sperm ejaculated, and that male mate-order reduces sperm numbers. Male sperm numbers drop significantly from one mating to the next, and this has implications for sperm competiveness, as Thamnophis sirtalis exhibits a disassociated reproductive tactic, in that sperm stores are produced outside the breeding season, and thus cannot be replenished after mating. Interestingly, however, the on average the mobility of the sperm increased for a male's second mating. Therefore, increased sperm quality may compensate for reduced numbers in a competitive context. Further, females increase their remating rate when mating with males that are unable to deliver sperm. In chapter five, "Sexual conflict during mating in red-sided garter snakes as evidenced by genital manipulation", we revisited the CP in the context of sexual conflict. Sex-differences in optimal copulation duration can be a source of conflict, as increased copulation duration may be advantageous for males as it delays female remating. Males of many species actively guard females to prevent them from remating, and in some cases males produce copulatory plugs to prevent remating. If precopulatory choice is limited at the time of her first mating, conflict may be especially onerous to a female. The size of the plug is influenced by the copulation duration. We experimentally tested the contribution of male and female control over copulation duration. We ablated the largest basal spine on the male's hemipene and found a reduction in copulation duration and an increase in the variation of plug mass. Further, we anesthetized the female's cloaca and found copulation duration increased, which suggests that males benefit from increased copulation duration while females actively try to reduce copulation duration. Therefore, sexual conflict is manifest in divergent copulation duration optima for males and females.
Graduation date: 2013

Male pregnancy is a complex and energetically costly form of male parental care found exclusively in the fish family Syngathidae, which includes pipefishes, seahorses, and seadragons. The novelty of the male brood pouch raises questions about how this trait evolved and what role it plays in sexual selection. One possibility is that brood pouch evolution was partially shaped by postcopulatory sexual selection. We used the sexually dimorphic Gulf pipefish, Syngnathus scovelli, to test for postcopulatory sexual selection within broods and tradeoffs between successive male pregnancies as a function of female attractiveness. Offspring survivorship within a pregnancy was affected by the size of a male's mate, the number of eggs transferred, and the male's mating history. These results indicate the males invest more resources into broods from large, attractive mates to the detriment of future broods. Next, we investigated the effects of food limitation on male parental care strategies. Our data suggests that male Gulf pipefish sacrifice investment in future reproduction, via somatic growth, in favor of current reproduction. A positive relationship between number of failed eggs and male growth rate in our low-food treatments suggests that males may derive an energetic benefit from unsuccessful eggs in the brood pouch. Finally, we used a paired design, to investigate the effect of perceived female attractiveness on offspring survivorship. We found that, in general, males prefer the largest female available. Within a replicate, we found that the male that preferred their mate more, regardless of stimulus female size, also had higher offspring survivorship in the resulting brood. This result is exciting because it shows not only that cryptic male choice affects offspring survivorship in Gulf pipefish but also that mate preference can have a prolonged effect on an individual’s reproductive success. Ultimately, our data suggests that the evolution of the brood pouch has produced a trait that not only nurtures the offspring but also exert cryptic male choice.

Darwin identified sexual selection as an important evolutionary process resulting from differences among males in their ability to secure mates. In the latter half of the 20th century, it became apparent that females often mate with multiple partners within the same reproductive cycle, leading to the overlap of ejaculates from multiple males and sperm competition for the fertilization of the eggs. Here, I examine how sperm competition has influenced the evolution of Xiphophorus nigrensis, an internally fertilized, livebearing fish with alternative male mating tactics that are dependent upon male size. I find that variation in male tactic is correlated with variation in traits relevant to sperm competition: small males that sneak copulations produce ejaculates with a greater proportion of fertilization-capable sperm (sperm viability) and sperm that is longer-lived following activation compared to large males that court females. Sperm morphology is also divergent between tactics and correlated with sperm performance: smaller males have larger midpieces and midpiece size is positively correlated with sperm velocity and longevity. Social environment also affects ejaculate quality, with sperm velocity rapidly increasing when a small male is exposed to another small male compared to when he is exposed to a large male. Large male ejaculates were invariant across social environments. Next, I demonstrate experimentally that the observed variation in sperm quality has important consequences for the outcome of sperm competition. Males with superior sperm viability sire more offspring, while sperm velocity is negatively associated with sperm competitive ability when sperm are stored within the female prior to fertilization. Finally, I show that sperm competition is likely to have important effects on male reproductive success in the wild by characterizing the genetic mating system of X. nigrensis. I find that 61% of females collected from the Nacimiento Río Choy produce offspring sired by 2-4 males. Paternity is strongly skewed among sires, with an average of 70% of offspring sired by one of the males represented in the brood. These studies illustrate sperm competition can have potent effects on the evolution of animals.
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