Cosa succede dopo la copula? La competizione spermatica raccontata dai pesci di Trinidad

Una delle forze che più sorprendentemente alimentano l’evoluzione è la selezione sessuale. Questa appare negli animali nella sua massima complessità: la selezione avviene in un contesto in cui due o più individui, spesso maschi e femmine, interagiscono, cooperano e lottano. Ma fra questi solo alcuni, alla fine, sono in grado di lasciare discendenti. Queste interazioni possono avvenire in momenti diversi del rapporto che si instaura fra individui e uno degli spartiacque temporali più importanti è la copula. Mentre la selezione che avviene prima della copula favorisce alcuni individui piuttosto che altri, quella che avviene fra copula e fecondazione delle uova agisce invece per lo più sui gameti. Si parla in questo caso di selezione sessuale postcopulatoria. Due processi distinti entrano in gioco a questo punto: la competizione spermatica (quando gli spermi di individui differenti competono per fecondare le stesse uova) e la scelta criptica femminile (quando le femmine sono in grado di favorire alcuni spermi a scapito di altri). Nel capitolo viene descritta la competizione spermatica, spiegando quali adattamenti ha promosso e in che modo può influenzare i processi evolutivi. Verrannopresentate le ultime ricerche in questo ambito con particolare attenzione a quanto scopertoin una classe di pesci tropicali, i Poecilidi

Possible glimpses into early speciation: the effect of ovarian fluid on sperm velocity accords with post-copulatory isolation between two guppy populations.

Identifying mechanisms of reproductive isolation is key to understanding speciation. Among the putative mechanisms underlying reproductive isolation, sperm-female interactions (postmating-prezygotic barriers) are arguably the hardest to identify, not least because these are likely to operate at the cellular or molecular level. Yet sperm-female interactions offer great potential to prevent the transfer of genetic information between different populations at the initial stages of speciation. Here we provide a preliminary test for the presence of a putative postmating-prezygotic barrier operating between three populations of Trinidadian guppies (Poecilia reticulata), an internally fertilizing fish that inhabits streams with different levels of connectivity across Trinidad. We experimentally evaluate the effect of female ovarian fluid on sperm velocity (a predictor of competitive fertilization success) according to whether males and females were from the same (native) or different (foreign) populations. Our results reveal the potential for ovarian fluid to act as a postmating-prezygotic barrier between two populations from different drainages, but also that the strength of this barrier is different among populations. This result may explain the previous finding that, in some populations, sperm from native males have precedence over foreign sperm, which could eventually lead to reproductive isolation between these populations. This article is protected by copyright. All rights reserved

Chemical signals from eggs facilitate cryptic female choice in humans

Mate choice can continue after mating via chemical communication between the female reproductive system and sperm. While there is a growing appreciation that females can bias sperm use and paternity by exerting cryptic female choice for preferred males, we know surprisingly little about the mechanisms underlying these post-mating choices. In particular, whether chemical signals released from eggs (chemoattractants) allow females to exert cryptic female choice to favour sperm from specific males remains an open question, particularly in species (including humans) where adults exercise pre-mating mate choice. Here, we adapt a classic dichotomous mate choice assay to the microscopic scale to assess gamete-mediated mate choice in humans. We examined how sperm respond to follicular fluid, a source of human sperm chemoattractants, from either their partner or a non-partner female when experiencing a simultaneous or non-simultaneous choice between follicular fluids. We report robust evidence under these two distinct experimental conditions that follicular fluid from different females consistently and differentially attracts sperm from specific males. This chemoattractant-moderated choice of sperm offers eggs an avenue to exercise independent mate preference. Indeed, gamete-mediated mate choice did not reinforce pre-mating human mate choice decisions. Our results demonstrate that chemoattractants facilitate gamete-mediated mate choice in humans, which offers females the opportunity to exert cryptic female choice for sperm from specific males

Sexual selection in Poecilia reticulata: the maintenance of variability in male pre- and postcopulatory sexual traits

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

Data from: Directional postcopulatory sexual selection is associated with female sperm storage in Trinidadian guppies

Female sperm storage (FSS) is taxonomically widespread and often associated with intense sperm competition, yet its consequences on postcopulatory sexual selection (PCSS) are poorly known. Theory predicts that FSS will reduce the strength of PCSS, because sperm characteristics favored before and after FSS may be traded-off, and opportunities for nondirectional PCSS should increase. We explored these questions in the guppy (Poecilia reticulata), by allowing females to mate multiply and by comparing the paternity pattern in two successive broods. Contrary to predictions, the variance in male fertilization success increased after FSS, driven by a change in male paternity share across broods. This change was positively associated with sperm velocity (measured before FSS) but not with the duration of FSS, indirectly suggesting that faster sperm were better in entering female storage organs, rather than in persisting within them. Other male traits, such as male size and orange color, heterozygosity, and relatedness to the female, did not influence paternity after FSS. These results indicate that processes associated with FSS tend to reinforce the strength of PCSS in guppies, rather than weaken it. Further work is necessary to test whether this pattern changes in case of more prolonged FSS

Data from: Cross–generational effects of sexual harassment on female fitness in the guppy

A large number of studies have identified several direct costs of sexual harassment, including energy expenditure and reduced foraging ability. However, the fitness consequences of sexual harassment over a longer time-scale have never been investigated. Here, we estimated the effects of male sexual harassment on female fitness in the guppy, Poecilia reticulata, a small tropical fish in which sexual conflict over mating rates is particularly pronounced. We compared the lifetime fecundity and survival of two groups of females exposed to different levels of sexual harassment. We further estimated the effect of sexual harassment on the fitness of the second generation by raising the offspring to maturity and measuring traits associated with fecundity in daughters and with pre- and post-copulatory competitiveness in sons. Although sexual harassment did not reduce mothers’ lifetime fecundity, it affected their timing of reproductive allocation. Interestingly, sexually harassed females produced daughters with smaller body size and sons that were less attractive to females and less successful in achieving coercive copulations than the sons of control females. This study provides compelling evidence that sexual harassment can have negative cross-generational fitness effects, suggesting that its consequences on female fitness may be more profound than currently thought

CROSS-GENERATIONAL EFFECTS OF SEXUAL HARASSMENT ON FEMALE FITNESS IN THE GUPPY

Sexual 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