On the selective interplays in an acoustic moth : a study of the origin, the evolution and the maintenance of sexual behaviours

Pour comprendre comment la sélection naturelle modèle les traits sexuels, l’emploi d’une approche intégrative des processus sélectifs en jeu semble aujourd’hui indispensable. Durant ma thèse je me suis ainsi intéressé aux influences simultanées des sélections de viabilité et sexuelle sur l’origine, l’évolution et le maintien des traits sexuels de la petite teigne de la ruche (Achroia grisella). Chez cette pyrale les mâles se regroupent en leks, produisent un chant d’appel ultrasonique intense et les femelles choisissent un partenaire sexuel en se basant sur des caractéristiques acoustiques spécifiques de ce chant. Cependant les signaux sexuels ultrasoniques des mâles peuvent également attirer des prédateurs : les chauves-souris insectivores. Ainsi, au sein des leks, les sélections sexuelle et de viabilité jouent et peuvent modeler (1) l’évolution du choix des femelles, (2) le maintien et l’évolution du lek, (3) l’origine de la communication acoustique sexuelle. Les travaux conduits durant cette thèse soulignent l’intérêt de l’étude du jeu des sélections sexuelle et de viabilité pour comprendre comment la sélection naturelle peut modeler l’origine, l’évolution et le maintien des traits sexuels. Les résultats indiquent en particulier le rôle crucial de la pression de prédation dans ces processus sélectifs.In order to achieve a better understanding of how natural selection shapes sexual traits it is essential to consider the interplay of the various selective processes at work. For my thesis I investigated the simultaneous influences of viability and sexual selections on the origin, the evolution and the maintenance of sexual traits in the lesser waxmoth Achroia grisella. Females of this pyralid moth choose their mate based on acoustic characters of the ultrasonic calling song broadcasted by males while competing at lek. However male ultrasonic displays are very conspicuous and may attract specific predators: insectivorous bats. Therefore at leks sexual and viability selection pressures act simultaneously and can shape (1) the evolution of female mate choice, (2) the maintenance and evolution of lekking, (3) the origin of sexual acoustic communication. Taken as a whole this work emphasises the relevance of the study of selective interplays between viability and sexual selections in order to improve our understanding of how natural selection may shape the origin, evolution and maintenance of sexual traits. In particular results indicate the crucial role played by predation pressure within these evolutionary processes

Economics of mate choice at leks: do female waxmoths pay costs for indirect genetic benefits?

International audienceSexual selection theory predicts low costs of choice when females choose among males for genetic (indirect) benefits, as occurs at leks. However, few empirical studies have investigated the actual costs incurred during the process of pair formation, and we generally do not know whether and to what extent females incur energetic expenditure, exposure to predation, or simple allocation of time by virtue of their choosiness. Do females that choose mates at larger aggregations of males necessarily pay these costs? Moreover, what costs are they willing to pay to obtain potential benefits? We addressed these questions in an acoustic pyralid moth, Achroia grisella, in which males aggregate and attract females with an advertisement song. Female choice is based on acoustic characters of displaying males, and only genetic benefits appear to be available. We measured the movement and time that females spent in mate sampling when presented with varying numbers of males in a laboratory arena. We found that female choice for specific males was retained as male number increased, although their sampling effort increased: female trajectories lengthened and reversed direction more often. The repeatability of female choice at larger leks and the basic precision of female phonotaxis indicated that the lengthened trajectories reflected sampling and choosiness as opposed to confusion. We propose that the cost of such choosiness in natural populations may be an increased exposure to predation and that females pay this cost because of the opportunity to mate with a specific male with certain song characteristics. Key words: acoustic communication, mating signals, orientation, pair formation, sexual selection

Du jeu des sélections chez une pyrale musicienne (étude de l'origine, de l'évolution et du maintien sélectif des comportements sexuels)

Pour comprendre comment la sélection naturelle modèle les traits sexuels, l emploi d une approche intégrative des processus sélectifs en jeu semble aujourd hui indispensable. Durant ma thèse je me suis ainsi intéressé aux influences simultanées des sélections de viabilité et sexuelle sur l origine, l évolution et le maintien des traits sexuels de la petite teigne de la ruche (Achroia grisella). Chez cette pyrale les mâles se regroupent en leks, produisent un chant d appel ultrasonique intense et les femelles choisissent un partenaire sexuel en se basant sur des caractéristiques acoustiques spécifiques de ce chant. Cependant les signaux sexuels ultrasoniques des mâles peuvent également attirer des prédateurs : les chauves-souris insectivores. Ainsi, au sein des leks, les sélections sexuelle et de viabilité jouent et peuvent modeler (1) l évolution du choix des femelles, (2) le maintien et l évolution du lek, (3) l origine de la communication acoustique sexuelle. Les travaux conduits durant cette thèse soulignent l intérêt de l étude du jeu des sélections sexuelle et de viabilité pour comprendre comment la sélection naturelle peut modeler l origine, l évolution et le maintien des traits sexuels. Les résultats indiquent en particulier le rôle crucial de la pression de prédation dans ces processus sélectifs.In order to achieve a better understanding of how natural selection shapes sexual traits it is essential to consider the interplay of the various selective processes at work. For my thesis I investigated the simultaneous influences of viability and sexual selections on the origin, the evolution and the maintenance of sexual traits in the lesser waxmoth Achroia grisella. Females of this pyralid moth choose their mate based on acoustic characters of the ultrasonic calling song broadcasted by males while competing at lek. However male ultrasonic displays are very conspicuous and may attract specific predators: insectivorous bats. Therefore at leks sexual and viability selection pressures act simultaneously and can shape (1) the evolution of female mate choice, (2) the maintenance and evolution of lekking, (3) the origin of sexual acoustic communication. Taken as a whole this work emphasises the relevance of the study of selective interplays between viability and sexual selections in order to improve our understanding of how natural selection may shape the origin, evolution and maintenance of sexual traits. In particular results indicate the crucial role played by predation pressure within these evolutionary processes.TOURS-Bibl.électronique (372610011) / SudocSudocFranceF

The complex auditory scene at leks: balancing antipredator behaviour and competitive signalling in an acoustic moth

International audienceLepidoptera life history theory pyralid moth sexual selection trade-off ultrasound signal Although sexual activity in many animal species is reduced when predation pressure intensifies, such reduction may be attenuated in accordance with age, demography or sexual competition. For example, males in lekking aggregations might forgo evasive behaviour and continue their signalling activity when exposed to predation for various reasons: the pressure to engage in signal competition with neighbours outweighs the risk of a predator attack, the per capita risk of attack is lower on larger leks, signals from neighbours within the lek mask predator cues, or limitations on general attention prevent a lekking male from simultaneously signalling and monitoring predators. We addressed the problem of balancing antipredator behaviour and signal competition in an acoustic pyralid moth, Achroia grisella, in which males gather in leks and broadcast an ultrasonic mating call. There is evidence that A. grisella can be menaced by substrate-gleaning bats and that singing males generally become silent upon perceiving bat echolocation signals or pulsed ultrasound bearing the characteristics of these signals. In this study, the incidence and duration of these silence responses were greatly reduced in lekking males compared with solitary individuals. Moreover, a moderate reduction in silence responses persisted when we broadcast, to individual males, song from a lek followed by bat echolocation stimuli. Thus, while signal masking may play a role in attenuating antipredator behaviour in lekking males, other factors, including signal competition and dilution of predation pressure, are probable influences as well. Studies of mating behaviour in both vertebrate and invertebrate species commonly note marked reductions or changes in sexual activity in the presence of predators (Burk 1982; Magnhagen 1991; Fuller & Berglund 1996). Because male signalling is often conspicuous to natural enemies as well as to females (Zuk & Kolluru 1998), males are expected to broadcast their advertisements at reduced intensity, intermittently or not at all when predators are perceived. Similarly, the orientation movements of both sexes during pair formation may reveal their presence to third parties (eavesdrop-pers) and females may therefore be less receptive to males and male signals (Farris et al. 1998; Dill et al. 1999; Jones et al. 2002), or discriminate less among local males (Hedrick & Dill 1993; Danchin & Cézilly 2005), if predation intensifies. Courtship and copulation pose additional risks (Sih et al. 1990; Koga et al. 1998; but see Gwynne 1989 for data indicating an absence of risk) and may also be shortened, or avoided and deferred until a safer moment. The attention to one's partner that normally occurs during courtship may be incompatible with the vigilance necessary to monitor predators, and the immobility during copulation may render escape from predators difficult or impossible. These expectations are general predictions, which may be modified in accordance with the principles of life history theory (Candolin 1998). For example, as animals age and the expected number of future mating opportunities diminishes, the decision equation that modulates the conflicting demands of current reproduction versus survival and the possibility of future reproduction may change such that males continue signalling and females remain receptive and orient towards signalling males under higher levels of perceived predation (Lafaille et al. 2010). Thus, individuals of either sex would not forgo terminal mating opportunities under some conditions (Clutton-Brock 1984). Social behaviour and the competition inherent within groups introduce the possibility of additional modifications to the partitioning of effort between current reproduction versus survival and potential future reproduction. From the male perspective, when individuals advertise in the vicinity of conspecifics, the phenomenon of signal competition arises in which each male may be under pressure at least to match the broadcasts of his neighbour

Data from: Foraging bumblebees use social cues more when the task is difficult

When foraging in their natural environment, many animals readily complement their personal knowledge with additional social information. To balance the costs and benefits of copying others, animals have to discern situations in which it is more advantageous to use social rather than personal information. Here, we used foraging bumblebees (Bombus terrestris) in a controlled laboratory setting and showed that the difficulty of a foraging task affects how the bees weight the two types of information. We used artificial flowers to devise easy and difficult discriminatory tasks, and tested the influence of floral and social cues on decision making. When facing an easy discrimination task, foraging bees were likely to rely on personal information and were only marginally affected by social information. By contrast, they prioritized social over personal information when flower discrimination was difficult and therefore the probability of making errors was higher. In summary, bees are able to use social and personal information to optimize foraging decisions in a flexible way

The dilemma of Fisherian sexual selection: Mate choice for indirect benefits despite rarity and overall weakness of trait-preference genetic correlation

International audienceFisher's mechanism of sexual selection is a fundamental element of evolutionary theory. In it nonrandom mate choice causes a genetic covariance between a male trait and female preference for that trait and thereby generates a positive feedback process sustaining accelerated coevolution of the trait and preference. Numerous theoretical models of Fisher's mechanism have confirmed its mathematical underpinnings, yet biologists have often failed to find evidence for trait-preference genetic correlation in populations in which the mechanism was expected to function. We undertook a survey of the literature to conduct a formal meta-analysis probing the incidence and strength of trait-preference correlation among animal species. Our meta-analysis found significant positive genetic correlations in fewer than 20% of the species studied and an overall weighted correlation that is slightly positive. Importantly, a significant positive correlation was not found in any thorough study that included multiple subgroups. We discuss several ways in which the dynamic, multivariate nature of mate choice may reduce the trait-preference genetic correlation predicted by Fisher's mechanism. We then entertain the possibilities that Fisherian-like processes sometimes function without genetic correlation, and that mate choice may persist in a population as long as genetic correlation, and therefore Fisher's mechanism, occurs intermittently

What determines lek size? Cognitive constraints and per capita attraction of females limit male aggregation in an acoustic moth

International audienceIt has been proposed that leks arise because of increased mating benefits in aggregations of displaying males, and some evidence supports this hypothesis. But observations also indicate that lekking aggregations include only a small percentage of the males in a population, implying that certain factors limit lek size. Potential factors include increasing travel costs to find and form large but distant aggregations, greater attraction of predators and higher levels of aggression. Any one of these constraints may cause the number of females arriving at larger leks to decelerate such that per capita male attractiveness, and hence mating success, declines above an optimum lek size. None the less, relatively little empirical workhas examined what determines lek size. In particular the possibility that cognitive aspects might constrain lek size has rarely been considered. We studied this question in Achroia grisella, an acoustic moth in which singing males form small aggregations that attract females. We created artificial leks in the laboratory and tested their relative attractiveness to females; we also tested male preferences to form and join such aggregations. Females preferred male aggregations over solitary singers, but the marginal per capita attractiveness of an aggregation of n þ 2 males versus n males waned for n 5. Similarly we found that males were attracted to other males singing in the vicinity, but this effect disappeared for n 4. We infer that lek size is limited because the marginal per capita attractiveness of larger leks only occurs for small groups. This constraint probably arises because females distinguish leks by overall song rate but are neuroethologically incapable of discriminating rates above a threshold value corresponding to groups of four to six males. These findings emphasize the critical role that neural constraints may play in determining fundamental parameters of complex behaviours such as lekking

Bat predation and the evolution of leks in acoustic moths

International audienceTheories of lek evolution generally invoke enhanced mating success experienced by males signalling in aggregations. Reduced predation has also been acknowledged as a potential factor driving lek formation, but its role is more ambiguous. Although lekking is a complex behaviour, few empirical studies have investigated the role of both claims. We studied the potential pressures imposed by mating success and predation in an acoustic moth, Achroia grisella, in which males gather in leks and broadcast a calling song attractive to females. We exploited the ability to manipulate the distribution of singing males in laboratory arenas to create different-sized leks and tested female preferences for these aggregations. Because A. grisella are vulnerable to predation by bats while in flight and on the substrate, we also tested the responses of a potential predator, Rhinolophus ferrumequinum, a bat species that feeds on moths, to the experimental leks. We found that the per capita attractiveness of A. grisella males to females rose with increasing lek size. R. ferrumequinum also oriented toward experimental A. grisella leks, but this attraction did not increase at larger leks. Thus, a male's per capita exposure to predation risk declined as more moths joined the lek. A. grisella males appear to benefit from advertising in larger leks in terms of both increased mate attraction and reduced predation risk. Our results support the idea that multiple factors operating simultaneously may maintain lekking behaviour