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. / text

Polygyny is the most common mating system in mammalian species (95%), yet our understanding of polygynous systems and microevolutionary processes is still limited. Pinniped mating systems range from extreme polygyny (e.g. elephant seals) to sequential female defence by males and hence have often been used as models for mating system studies. Parentage analysis has enabled the examination of mating success, the identification of pedigrees, and the elucidation of social organisation, greatly enhancing our understanding of mating systems (Chapter 1). However, such analyses are not without pitfalls, with erroneous assignments common in open systems (i.e. when parental and offspring samplings are incomplete). We investigated the effects of the user-defined parameters on the accuracy of parental assignment using two commonly used parental allocation programme, CERVUS and PASOS (Chapter 2). We showed that inaccurate user-defined parameters in CERVUS and PASOS can lead to highly biased output e.g. the assignment rate at 95% CL of offspring with a sampled known mother to sampled males decreased from 58% to 32% when the proportion of candidate males sampled in the parameter options decreasing 4-fold. We found that the use of both CERVUS and PASOS for parentage assignment can increase the likelihood of correctly allocating offspring to sampled parents to 97% in our study system. Incorrect parental assignment can bias estimates of various biological parameters, such as lifetime reproductive success and mate choice preference, and hence bias ecological and evolutionary interpretations. Here, we propose solutions to increase the power of parentage assignment and hence decrease the bias in biological parameter estimates. In addition, we analysed the effects of the intrinsic bias in likelihood assignment approaches towards assigning higher probability of parentage on individuals with rare alleles and those with heightened offspring-parent matches, which increase with the number of homozygous loci (Chapter 3). We showed that, as a consequence of the algorithms employed in the programmes CERVUS and PASOS, heterozygote males with rare genotypes are assigned higher rates of parentage than males with common alleles. Consequently, where two males could both be biological fathers of a given offspring, parentage assignment will more often go to the male with the rarer alleles (most often in heterozygous loci). Thus, the commonly used parentage assignment methods may systematically bias the results of parentage analyses towards supporting the notion that females prefer more genetically unusual, most often heterozygous, males. Such a bias may sway investigators towards incorrectly supporting the concept that females choose genetically more unusual males for heterozygosity fitness benefits that underpin the good genes hypothesis, when in fact no such relationship may exist. In polygynous mammals, successful males mate with multiple females by competing with and limiting the access of other males to females. When the status of many males (age, size, health, genetic etc.) prevents them from achieving the primary mating tactic, theory predicts selection for a diversification of male mating tactics. Recent studies in pinnipeds have shown that observed male mating success was correlated to male paternity success in some species (elephant-seals), but not in others (grey seals). The existence of alternative mating strategies can explain those discrepancies. Chapter 4 implemented the guidelines provided in Chapter 2 and 3 and focused on the polygynous New Zealand fur seal Arctocephalus forsteri, predicting that 1) competition for females is likely to cause a diversification of male mating tactics; and 2) that alternative tactics can yield reproductive success. Our results indicated three male behavioural profiles; one corresponded to large territorial males and two illustrated a continuum of alternative tactics employed by non-territorial subordinate males. Our study highlights that holding a territory is not a necessary condition for reproductive success in a population of otariids. The degree of sexual size dimorphism in polygynous species is expected to increase with the degree of intra-sexual competition and in turn with the degree of polygyny. The life history of an individual is the pattern of resource allocations to growth, maintenance, and reproduction throughout its lifetime. Both females and males incur viability costs of mating and reproduction. However, male viability costs due to increase growth and male-male competition can be greater than female viability costs of mate choice and reproduction. Although an abundant literature on sexual dimorphism in morphology, physiology, and parasite infections is available, little is known on the intra-sexual differences in physiology and parasite infections associated to the reproductive success of different mating strategies in mammalian species. Chapter 5 examined the reproductive costs between territorial and subordinate males New Zealand fur seal related to their relative reproductive success using a multidisciplinary approach (behaviour, genetics, endocrinology, parasitology). We found that dominant New Zealand fur seal males endure higher reproductive costs due to the direct and indirect effects of high testosterone levels and parasite burdens. Our study highlights that holding a territory confers a higher reproductive success, but induces higher costs of reproduction that may impair survival. Understanding microevolutionary processes associated to polygynous systems is fundamental in light of the ongoing anthropogenic alteration of the environment through climatic variations and habitat reduction which ultimately affect opportunity for sexual selection and shape the life history trade-offs.

Polygyny is the most common mating system in mammalian species (95%), yet our understanding of polygynous systems and microevolutionary processes is still limited. Pinniped mating systems range from extreme polygyny (e.g. elephant seals) to sequential female defence by males and hence have often been used as models for mating system studies. Parentage analysis has enabled the examination of mating success, the identification of pedigrees, and the elucidation of social organisation, greatly enhancing our understanding of mating systems (Chapter 1). However, such analyses are not without pitfalls, with erroneous assignments common in open systems (i.e. when parental and offspring samplings are incomplete). We investigated the effects of the user-defined parameters on the accuracy of parental assignment using two commonly used parental allocation programme, CERVUS and PASOS (Chapter 2). We showed that inaccurate user-defined parameters in CERVUS and PASOS can lead to highly biased output e.g. the assignment rate at 95% CL of offspring with a sampled known mother to sampled males decreased from 58% to 32% when the proportion of candidate males sampled in the parameter options decreasing 4-fold. We found that the use of both CERVUS and PASOS for parentage assignment can increase the likelihood of correctly allocating offspring to sampled parents to 97% in our study system. Incorrect parental assignment can bias estimates of various biological parameters, such as lifetime reproductive success and mate choice preference, and hence bias ecological and evolutionary interpretations. Here, we propose solutions to increase the power of parentage assignment and hence decrease the bias in biological parameter estimates. In addition, we analysed the effects of the intrinsic bias in likelihood assignment approaches towards assigning higher probability of parentage on individuals with rare alleles and those with heightened offspring-parent matches, which increase with the number of homozygous loci (Chapter 3). We showed that, as a consequence of the algorithms employed in the programmes CERVUS and PASOS, heterozygote males with rare genotypes are assigned higher rates of parentage than males with common alleles. Consequently, where two males could both be biological fathers of a given offspring, parentage assignment will more often go to the male with the rarer alleles (most often in heterozygous loci). Thus, the commonly used parentage assignment methods may systematically bias the results of parentage analyses towards supporting the notion that females prefer more genetically unusual, most often heterozygous, males. Such a bias may sway investigators towards incorrectly supporting the concept that females choose genetically more unusual males for heterozygosity fitness benefits that underpin the good genes hypothesis, when in fact no such relationship may exist. In polygynous mammals, successful males mate with multiple females by competing with and limiting the access of other males to females. When the status of many males (age, size, health, genetic etc.) prevents them from achieving the primary mating tactic, theory predicts selection for a diversification of male mating tactics. Recent studies in pinnipeds have shown that observed male mating success was correlated to male paternity success in some species (elephant-seals), but not in others (grey seals). The existence of alternative mating strategies can explain those discrepancies. Chapter 4 implemented the guidelines provided in Chapter 2 and 3 and focused on the polygynous New Zealand fur seal Arctocephalus forsteri, predicting that 1) competition for females is likely to cause a diversification of male mating tactics; and 2) that alternative tactics can yield reproductive success. Our results indicated three male behavioural profiles; one corresponded to large territorial males and two illustrated a continuum of alternative tactics employed by non-territorial subordinate males. Our study highlights that holding a territory is not a necessary condition for reproductive success in a population of otariids. The degree of sexual size dimorphism in polygynous species is expected to increase with the degree of intra-sexual competition and in turn with the degree of polygyny. The life history of an individual is the pattern of resource allocations to growth, maintenance, and reproduction throughout its lifetime. Both females and males incur viability costs of mating and reproduction. However, male viability costs due to increase growth and male-male competition can be greater than female viability costs of mate choice and reproduction. Although an abundant literature on sexual dimorphism in morphology, physiology, and parasite infections is available, little is known on the intra-sexual differences in physiology and parasite infections associated to the reproductive success of different mating strategies in mammalian species. Chapter 5 examined the reproductive costs between territorial and subordinate males New Zealand fur seal related to their relative reproductive success using a multidisciplinary approach (behaviour, genetics, endocrinology, parasitology). We found that dominant New Zealand fur seal males endure higher reproductive costs due to the direct and indirect effects of high testosterone levels and parasite burdens. Our study highlights that holding a territory confers a higher reproductive success, but induces higher costs of reproduction that may impair survival. Understanding microevolutionary processes associated to polygynous systems is fundamental in light of the ongoing anthropogenic alteration of the environment through climatic variations and habitat reduction which ultimately affect opportunity for sexual selection and shape the life history trade-offs.

京都大学 / 0048 / 新制・課程博士 / 博士(理学) / 甲第20048号 / 理博第4233号 / 新制||理||1609(附属図書館) / 京都大学大学院理学研究科生物科学専攻 / (主査)教授 中川 尚史, 教授 沼田 英治, 教授 中務 真人 / 学位規則第4条第1項該当 / Doctor of Science / Kyoto University / DFAM

No description available.

The processes and mechanisms that govern brain size evolution remain a widely discussed topic in evolutionary biology. How relative brain size relates to animal behaviour and cognition is even more controversial. Recent comparative and experimental studies have shown a positive relationship between relative brain size and complexity of behaviour. Some of the most important behaviours that have direct consequences for an individual’s fitness are reproductive behaviours, and they sometimes require quite complex behavioural repertoires. Selection for complex behaviour might therefore induce an expansion of brain size to allow for cognitively demanding tasks during courtship and mating. In the present study we investigated the effect of relative brain size on reproductive behaviour in male guppies (Poecilia reticulata), using fish from a recently established brain size artificial selection experiment. Females were paired with either a large- or a small-brained male, and we collected data on a suite of male courtship behaviours including sneak copulation attempts, courtship display, gonopodial swings and time spent following the female. Although the extent of orange colouration, a trait that varies across large- and small-brained males, affected male behaviour, we were not able to detect any difference in reproductive behaviour between the brain size selection lines. These results suggest that there is no strong association between male mating behaviour and relative brain size, and future studies will examine this question further. But currently, our results indicate that relative brain size might not be linked to reproductive behaviour to any significant extent, at least not in the guppy.

In meiner Dissertation untersuche ich das Paarungs- und Fortpflanzungsverhalten des Europäischen Grasfrosches (Rana temporaria) in einem evolutionären Kontext. Mein Ziel ist es zu verstehen, welche Mechanismen zur Bildung von Paaren führen, ob die Partnerwahl die Paarungsmuster erklärt, die wir beobachten können, und ob es evolutive Vorteile gibt, die sich aus der Paarung mit einem bestimmten Partner ergeben. Die Suche nach und die Konkurrenz um Paarungspartner führt zur Entwicklung verschiedener Paarungssysteme, Strategien und Taktiken, um den Reproduktionserfolg während der gesamten Lebensdauer zu erhöhen. Das Paarungsverhalten wird durch natürliche und sexuelle Selektion beeinflusst, wobei beide in unterschiedliche Richtungen wirken können. Für die meisten Individuen ist das Überleben unerlässlich, um sich so oft wie möglich zu reproduzieren, und dadurch die reproduktive Gesamtfitness zu erhöhen. Andererseits könnte ein auffälliges Verhalten bei der Fortpflanzung das Prädationsrisiko erhöhen. Der Akt der Paarung selbst kann bereits mit Risiken verbunden sein, welche sich auf die Überlebensraten auswirken können. Durch sexuelle Selektion könnten bestimmte sekundäre Geschlechtsmerkmale begünstigt werden, entweder aufgrund von Vorteilen im Wettbewerb innerhalb eines Geschlechts (intrasexuell), oder aufgrund spezifischer Präferenzen zwischen den Geschlechtern (intersexuelle Selektion). Damit sich die Partnerwahl entwickeln kann, muss der gewählte Paarungspartner Vorteile aufweisen, von denen der wählende Partner profitiert, denn die Wahl ist mit energetischen Kosten und zeitlichem Aufwand verbunden. Als Frühlaicher muss der Europäische Grasfrosch mit einem eingeschränktem Paarungszeitraum umgehen. Die Männchen konkurrieren um den Zugang zu Weibchen und es wird angenommen, dass sich Weibchen während der Paarung und Reproduktion passiv verhalten, da der hohe "Männchen-Überschuss" keine Wahl zulassen würde. Aus evolutionärer Sicht sollten Weibchen jedoch das wählerische Geschlecht sein und entscheiden mit wem sie sich paaren, da sie mehr Energie in die Eierproduktion investieren. / In my thesis, I examine the mating and reproductive behaviour of the European Common Frog (Rana temporaria) in an evolutionary context. I aim to understand which mechanisms lead to the formation of pairs, if mate choice shapes the patterns of mating that we can observe and if there are benefits derived from pairing with a specific mate. The search and competition for mating partners lead to the evolution of various mating systems, strategies and tactics to increase lifetime reproductive success. The mating behaviour is influenced by natural and sexual selection, whereby both could act in different directions. For most individuals, survival is essential in order to reproduce as often as possible to increase lifetime reproductive fitness. On the other hand, reproduction could increase predation risk due to conspicuous behaviour and risks associated with mating itself. Sexual selection could favour specific secondary sexual traits, either due to advantages in intrasexual competition, or by specific preferences of the choosy sex (intersexual selection). For mate choice to evolve, there need to be benefits associated with the chosen mating partner, because choosiness involves costs in terms of energy and time constraints during mating. As an explosive breeder, the European Common Frog has to deal with time constraints during the short breeding season. The males are competing for the access to females and it is assumed that females are passive during breeding due to a high male-biased operational sex ratio. However, from an evolutionary perspective females should be the choosy sex and should decide with whom to mate, as they invest more energy into the production of eggs.