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Devigili, Alessandro (2012) Sexual selection in Poecilia reticulata: the maintenance of variability in male pre- and postcopulatory sexual traits. [Tesi di dottorato]

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Abstract (inglese)

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’.

Abstract (italiano)

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.

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Tipo di EPrint:Tesi di dottorato
Relatore:Pilastro, Andrea
Dottorato (corsi e scuole):Ciclo 24 > Scuole 24 > BIOSCIENZE E BIOTECNOLOGIE > BIOLOGIA EVOLUZIONISTICA
Data di deposito della tesi:29 Gennaio 2012
Anno di Pubblicazione:29 Gennaio 2012
Parole chiave (italiano / inglese):Sexual selection; genetic variability; precopulatory sexual selection; postcopulatory sexual selection; Poecilia reticulata; condition dependence; genic capture hypothesis; sperm competition; multivariate selection
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/05 Zoologia
Struttura di riferimento:Dipartimenti > Dipartimento di Biologia
Codice ID:4405
Depositato il:15 Nov 2012 11:33
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