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Sexual conflict in the guppy, Poecilia reticulata
Full text linkSexual conflict is a widespread phenomenon in nature and it occurs over a wide range of decisions involving female-male interactions. This conflict drives the evolution of sexually antagonistic traits. Under a sexual conflict scenario, a trait that is beneficial to one sex is detrimental to the other driving the evolution of counteradaptation in a sort of ‘arm race’. In this process every evolutionary change in one sex is followed by a change in the opposite sex in order to minimize costs associated to the former. Mating frequency is one of the aspects of reproduction that could especially fuel sexual conflict and consequently sexually antagonistic coevolution because generally males have an optimal mating rate higher than females. My PhD thesis is aimed to study different aspects of sexual conflict using a small livebearing fish, Poecilia reticulata, as a model system. This species is particularly suitable for this purpose since sexual conflict is evident over mating rate, as revealed doubtless from the presence of high level of sexual harassment. I divided my researches into two main trends. First, I investigated costs and benefits of sexual conflict. Second, I focused on sexually antagonistic coevolution.
Costs and benefits of sexual conflict. Estimate costs and benefits of sexual conflict shed new light on the evolution of female resistance that is assumed to evolve to minimize the costs associated to superfluous matings. However, a recent hypothesis argues that female resistance evolves as a way to screen the more successful male and therefore operate via indirect benefits mechanism. Results from a study of the effects of sexual harassment on female’s lifetime fecundity and on offspring’s quality revealed that do not support this latter hypothesis. I demonstrated only costs of sexual harassment on offspring both in daughters and in sons. Moreover, study on heritability of males’ traits influencing reproductive success both at pre- and postcopulatory level revealed scarce sire heritability that instead is a fundamental assumption of the hypothesis. The low heritability for males’ traits may be explained by adaptive phenotypic plasticity that has been investigated for sperm velocity. This demonstrated an adjustment in sperm velocity by males according to mating opportunities.
Sexually antagonistic coevolution. My study of sexually antagonistic coevolution focuses on genitalia (male gonopodium and female oviduct). Gonopodial shape and dimension result important factors in determining the outcome of both consensual and coercive mating. Gonopodial length and shape resulted to be under sexual selection by female premating choice, with females mate more quickly with males possessing longer gonopodia with an enlarged shape. Gonopodium tip shape is revealed to be important in sperm transfer both in consensual and in forced matings. Another experiment demonstrated that females from low conflict population have minor control over sperm transfer in forced copulations by high conflict population males than relative counterparts. This result highlights the importance of male-female antagonistic coevolution in a sexual conflict scenario. An intraspecific study at population level corroborates this conclusion by providing evidence for a coevolutionary pattern between male and female concerning genitalia morphology. For this reason, genitalia might be the result of an evolutionary arm race between males and females in the struggle for control over mating rate and insemination success.Il conflitto sessuale è un fenomeno ubiquitario in natura e interessa molte delle interazioni maschio-femmina portando alla evoluzione di caratteristiche sessuali antagonistiche. Per definizione, nel conflitto sessuale una caratteristica che avvantaggia un sesso comporta dei costi per l’altro sesso, per cui di conseguenza in quest’ultimo viene favorita la comparsa di controadattamenti in una sorta di ‘corsa agli armamenti’, in cui ogni cambiamento evoluzionistico che appare in un sesso è seguito da un cambiamento nell’altro sesso volto a minimizzarne i costi. La frequenza degli accoppiamenti è uno degli aspetti cruciali in cui il conflitto sessuale si manifesta e porta alla selezione sessuale antagonistica perché in generale i maschi hanno una frequenza ottimale di accoppiamenti che è maggiore di quella delle femmine. La mia tesi di dottorato ha avuto lo scopo di studiare alcuni aspetti del conflitto sessuale utilizzando Poecilia reticulata come modello di studio. Questa specie è particolarmente adatta per lo studio di queste tematiche, dal momento che è evidente la presenza del conflitto sessuale per quanto riguarda il numero di accoppiamenti, come si evince chiaramente dall’alto livello di sexual harassment (i continui tentativi di copula da parte dei maschi) subito dalle femmine. Le ricerche che ho effettuato per la mia tesi di dottorato si possono suddividere in due filoni. Primo: costi e benefici del conflitto sessuale. Secondo: coevoluzione sessuale antagonistica.
Costi e benefici del conflitto sessuale. Studiare costi e benefici legati al conflitto sessuale è importante per capire l’evoluzione della resistenza femminile che si assume si sia evoluta con lo scopo di ridurre i costi legati agli accoppiamenti superflui. Di recente tuttavia si è avanzata l’ipotesi che la resistenza evolva attraverso il meccanismo dei benefici indiretti ottenuti selezionando i maschi più persistenti. Il primo lavoro ha riguardato lo studio degli effetti del sexual harassment sulla fecondità life-time delle femmine, ma anche degli effetti sulla prole. I risultati indicano che il costo del sexual harassment è visibile sulla prole, sia nei maschi che nelle femmine. Questi risultati non supportano perciò l’ipotesi che la resistenza femminile evolva attraverso l’acquisizione di benefici indiretti. Inoltre lo studio sull’ereditabilità di tratti maschili legati al successo riproduttivo ha dimostrato che tali caratteristiche sono poco ereditabili per via paterna, presupposto essenziale per questa ipotesi. La plasticità adattativa dei caratteri ne può spiegare la scarsa ereditabilità paterna riscontrata. Ho testato questa possibilità per un tratto legato al successo riproduttivo, la velocità spermatica, a seconda delle opportunità di accoppiamento percepite dal maschio. Si è dimostrato che i maschi sono in grado di modulare la velocità spermatica, confermando perciò la possibilità di un certo grado di plasticità che può spiegare i bassi valori di ereditabilità.
Coevoluzione sessuale antagonistica. Lo studio della coevoluzione sessuale antagonistica si è concentrato sulla morfologia dei genitali, sia maschili che femminili. I risultati indicano che la morfologia dell’organo copulatore influenza il successo nel maschio sia negli accoppiamenti cooperativi che in quelli forzati. In particolare la dimensione e la forma generale dell’organo copulatore sono sessualmente selezionati attraverso la scelta femminile, e le femmine si accoppiano più velocemente con maschi dotati di gonopodi più lunghi e di forma allargata. Anche la forma della parte più distale del gonopodio risulta importante nel determinare il trasferimento degli spermi.
La coevoluzione sessuale antagonistica prevede che quando una caratteristica modellata dal conflitto sessuale differisce tra popolazioni diverse, le femmine siano più resistenti ai maschi della propria popolazione, con cui si sono coevolute, rispetto a quelli di popolazioni diverse contro cui esse non hanno gli adattamenti necessari per resistere ad accoppiamenti non voluti.
Questa previsione è stata confermata attraverso uno studio su maschi e femmine di popolazioni a diverso conflitto sessuale, in cui è stato dimostrato che femmine poste con maschi provenienti da una popolazione con un maggiore grado di conflitto sessuale hanno un minor controllo sul trasferimento degli spermi, rispetto a femmine che hanno avuto la possibilità di coevolvere con tali maschi. Infine uno studio comparativo fra popolazioni diverse indica l’esistenza di coevoluzione tra genitali maschili e femminili, che varia a seconda del grado di conflitto sessuale a cui le popolazioni sono soggette. Per cui l’evoluzione dei genitali sembra essere il risultato di una corsa agli armamenti tra maschi e femmine per il controllo della frequenza degli accoppiamenti e del successo di inseminazione
Female control over multiple matings increases the opportunity for postcopulatory sexual selection
Full text linkIt is widely acknowledged that in most species sexual selection continues after mating. Although it is generally accepted that females play an important role in generating paternity biases (i.e., cryptic female choice), we lack a quantitative understanding of the relative importance of female-controlled processes in influencing variance in male reproductive fitness. Here we address this question experimentally using the guppy Poecilia reticulata, a polyandrous fish in which pre- and postcopulatory sexual selection jointly determine male reproductive fitness. We used a paired design to quantify patterns of paternity for pairs of rival males across two mating contexts, one in which the female retained full control over double (natural) matings and one where sperm from the same two males were artificially inseminated into the female. We then compared the relative paternity share for a given pair of males across both contexts, enabling us to test the key prediction that patterns of paternity will depend on the extent to which females retain behavioural control over matings. As predicted, we found stronger paternity biases when females retained full control over mating compared to when artificial insemination was used. Concomitantly, we show that the opportunity for postcopulatory sexual selection (standardised variance in male reproductive success) was greater when females retained control over double matings compared to when artificial insemination was used. Finally, we show that the paternity success of individual males exhibited higher repeatability across successive brood cycles when females retained behavioural control of matings compared to when AI was used. Collectively, these findings underscore the critical role that females play in determining the outcome of sexual selection and to our knowledge provide the first experimental evidence that behaviourally moderated components of cryptic female choice increase the opportunity for sexual selection
CROSS-GENERATIONAL EFFECTS OF SEXUAL HARASSMENT ON FEMALE FITNESS IN THE GUPPY
No full textSexual harassment is a common outcome of sexual conflict over mating rate. A large number of studies have identified several direct costs to females of sexual harassment including energy expenditure and reduced foraging ability. However, the fitness consequences of sexual harassment for descendants have rarely been investigated. Here, we manipulated the level of sexual harassment and mating rate in two groups of female guppies,Poecilia reticulata, a live-bearing fish in which sexual conflict over mating rate is particularly pronounced. Each female was allowed to interact with three males for one day (low sexual harassment, LSH) or for eight days (high sexual harassment, HSH) during each breeding cycle throughout their life. Female lifetime fecundity did not differ between the groups, but we found a strong effect on offspring fitness. HSH females produced (1) daughters with smaller bodies and (2) sons with shorter gonopodia, which were less attractive to females and less successful in coercive matings than their LSH counterparts. Although these results may be influenced by the indirect effects of sex ratio differences between treatments, they suggest that sexual harassment and elevated mating rate can have negative cross-generational fitness effects and more profound evolutionary consequences than currently thought
The role of female reproductive fluid in sperm competition
Full text linkThe role of non-gametic components of the ejaculate (seminal fluid) in fertility and sperm competitiveness is now well established. Surprisingly, however, we know far less about female reproductive fluid (FRF) in the context of sexual selection, and insights into male-FRF interactions in the context of sperm competition have only recently emerged. Despite this limited knowledge, evidence from taxonomically diverse species has revealed insights into the effects of FRF on sperm traits that have previously been implicated in studies of sperm competition. Specifically, through the differential effects of FRF on a range of sperm traits, including chemoattraction and alterations in sperm velocity, FRF has been shown to exert positive phenotypic effects on the sperm of males that are preferred as mating partners, or those from the most compatible or genetically diverse males. Despite these tantalizing insights into the putative sexually selected functions of FRF, we largely lack a mechanistic understanding of these processes. Taken together, the evidence presented here highlights the likely ubiquity of FRF-regulated biases in fertilization success across a diverse range of taxa, thus potentially elevating the importance of FRF to other non-gametic components that have so far been studied largely in males. This article is part of the theme issue 'Fifty years of sperm competition'
Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata)
No full textWhile both sperm number and quality are now recognized to be important in determining the outcome of sperm competition, very few studies have experimentally assessed the influence of these two parameters simultaneously. We studied the effect of sperm quality and number on competitive fertilization success in an internal-fertilizing fish, the guppy (Poecilia reticulata), which is characterized by high levels of sperm competition. We artificially inseminated virgin females with varying proportion of sperm from two competing males, while holding constant the total number of sperm transferred to the female. Sperm morphology and sperm swimming velocity were also determined prior to insemination. The paternity outcome of sperm competition trials was assessed through molecular analyses of the resulting offspring using polymorphic microsatellite loci. We found that both sperm number and sperm velocity affected the outcome of sperm competition, with males that contributed more and faster sperm achieving a greater paternity shar
Female guppies shorten brood retention in response to predator cues
No full textPredation risk influences the duration of offspring development in many species where embryos develop from externally shed eggs. Surprisingly, such predator-mediated effects on offspring development have rarely been explored in live-bearers. In this paper, we use the guppy (Poecilia reticulata), a live-bearing freshwater fish, to test whether the duration of brood retention (the time from mating to parturition) is influenced by experimental changes in the perceived level of predation. Because the swimming performance of female guppies is impaired during late pregnancy, we predicted that females would withhold broods for shorter periods when they are exposed to cues that signal a heightened risk of predation on adults rather than on juveniles. We therefore simulated increased risk of predation on adults by using a combination of pike-shaped models (resembling natural predators that prey on adult guppies) and 'alarm substances' derived from the skin extracts of adult conspecific females. Our results revealed that, under simulated predation risk, female guppies produced broods significantly more quickly than their counterparts assigned to a control group where predator cues were absent. A subsequent evaluation of offspring swimming performance revealed a significant positive association between neonate swimming speeds and the duration of brood retention, suggesting that by accelerating parturition, females may produce offspring with impaired locomotor skills. These findings, in conjunction with similar results from other live-bearing species, suggest that the conditions experienced by gestating females can generate significant variation in the timing of offspring development with potentially important implications for offspring fitness
Effects of ovarian fluid on sperm traits and its implications for cryptic female choice in zebrafish
Full text linkIn polyandrous mating systems, females maintain the opportunity to bias male fertilization success after mating in a process known as cryptic female choice. Mechanisms of cryptic female choice have been described both in internal and external fertilizers, and may affect fertilization processes at different stages before, during, and after fertilization. In internal fertilizers, females have substantial control over sperm storage and fertilization, whereas in external fertilizers, female control is limited. A key factor proposed to mediate cryptic female choice is the fluid surrounding the eggs, the ovarian fluid, as it may directly affect sperm performance. Here, we studied the role of ovarian fluid in post-mating sexual selection using the zebrafish, Danio rerio. Firstly, we assessed how ovarian fluid affects sperm swimming performance compared with freshwater. We focused on sperm motility, velocity, swimming trajectory, and longevity, all traits associated with competitive fertilization success in externally fertilizing fish. In a second step, we used a North Carolina II design to explore female, male, and female x male effects by testing sperm motility of 2 males in the ovarian fluid of 2 females in a total of 11 blocks. Our results indicate that the ovarian fluid affects sperm performance differently from freshwater. Specifically, sperm velocity, motility, and longevity were higher in the ovarian fluid than in freshwater, whereas sperm linearity and beat cross frequency showed the opposite pattern. Moreover, these effects varied according to male, female, and male x female identities, supporting the potential for cryptic female choice mediated by ovarian fluid in this species
Female presence influences sperm velocity in the guppy
No full textAs sperm production is costly, males are expected to strategically allocate resources to sperm production according to mating opportunities. While sperm number adjustments have been reported in several taxa, only a few studies investigated whether sperm quality shows adaptive plasticity as well. We tested this prediction in the guppy, Poecilia reticulata. A total of 46 males were initially stripped of all retrievable sperm before being randomly allocated to one of two treatments simulating different levels of mating opportunities (visual contact with females or female deprived). After 3 days, males were stripped and sperm velocity was assayed using Computer Assisted Sperm Analysis. Males in the presence of females produced significantly faster sperm than their counterparts. Implications for the evolution of this ejaculate plasticity in the light of results of sperm competition studies are discussed
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