Measuring natural and sexual selection on breeding values of male display traits in Drosophila serrata

Fundamental to many theories of sexual selection is the expectation that sexual traits, which males use in an attempt to increase mating success, confer costs as well as benefits to individual males. Although evolution of exaggerated male traits is predicted to be halted, by costs applied by natural selection, there is a lack of empirical work devoted to quantitatively establishing whether natural selection opposes sexual selection generated by the preferences of females. In this study, we quantified natural and sexual selection gradients on breeding values for cuticular hydrocarbon (CHC) components of male contact pheromones in Drosophila serrata. As male sexual traits may often be environmentally condition dependent, breeding values were used in the selection analysis to remove the possibility of environmental correlations between the measured trait and fitness biasing estimates of selection. The direction of natural selection was found to oppose sexual selection on a subset of CHCs examined. Opposing natural and sexual selection suggests that further evolution of the male pheromone may in part be limited by costs associated with attractive male CHC blends.

L’influence des capacités cognitives mâles et femelles sur le choix de partenaire chez le diamant mandarin (Taeniopygia guttata)

S’approvisionner en nourriture est essentiel à la survie et au succès reproducteur. Lorsque les animaux font face à des changements environnementaux brutaux, ils doivent s’ajuster rapidement à leur nouvel environnement et parfois même innover dans leur façon de s’approvisionner. Des processus comportementaux et cognitifs, tels que l’innovation et l’apprentissage, permettent aux animaux d'intégrer de nouveaux comportements à leur répertoire comportemental afin de s'adapter de façon optimale. Les performances cognitives varient entre les individus d’une même population et bien que des études récentes se soient intéressées aux causes de ce phénomène, de convaincantes évidences sont manquantes afin d’expliquer pourquoi ces variations sont maintenues. Au cours de ce mémoire, les questions des pressions de sélection s'exerçant sur les performances d’alimentation par une tâche motrice nouvelle sont abordées afin de mieux comprendre l'évolution des capacités cognitives au sein d'une population captive de diamants mandarins (Taeniopygia guttata). Nous avons tout d'abord testé si les femelles diamants mandarins modifient leurs préférences d'accouplement après avoir observé la performance d'alimentation par une tâche motrice nouvelle des mâles. Afin de déterminer si les femelles sont capables de discriminer entre les mâles sur la base de leur capacité cognitive, nous avons également évalué les performances d’apprentissage de chacune d’elles. En effet, des études ont suggéré qu’il peut être coûteux, spécialement en terme de temps, de discriminer entre des partenaires potentiels sur cette base. La généralisation d’une préférence pour un mâle performant à d’autres mâles possédant le même phénotype permettrait la réduction de ces coûts. Nous avons donc finalement testé si les femelles diamants mandarins peuvent généraliser leur préférence après avoir observé les performances d’alimentation pour une tâche motrice nouvelle d’un mâle. Nos résultats suggèrent que les femelles diamants mandarins ne peuvent évaluer les capacités cognitives d’un mâle par l’intermédiaire de traits indicateurs. Toutefois, nous avons démontré qu’une observation directe des performances d’alimentation d’un mâle guide le choix d’appariement des femelles. Également, nous avons montré que les femelles peuvent généraliser l’apparence du mâle le plus performant et utiliser cette information lors de l’évaluation de nouveaux mâles. La relation entre les performances cognitives et le choix de partenaire pourraient s’expliquer par exemple par une meilleure exploitation de l’habitat, mais nécessite des études plus approfondies.

L’influence des capacités cognitives mâles et femelles sur le choix de partenaire chez le diamant mandarin (Taeniopygia guttata)

S’approvisionner en nourriture est essentiel à la survie et au succès reproducteur. Lorsque les animaux font face à des changements environnementaux brutaux, ils doivent s’ajuster rapidement à leur nouvel environnement et parfois même innover dans leur façon de s’approvisionner. Des processus comportementaux et cognitifs, tels que l’innovation et l’apprentissage, permettent aux animaux d'intégrer de nouveaux comportements à leur répertoire comportemental afin de s'adapter de façon optimale. Les performances cognitives varient entre les individus d’une même population et bien que des études récentes se soient intéressées aux causes de ce phénomène, de convaincantes évidences sont manquantes afin d’expliquer pourquoi ces variations sont maintenues. Au cours de ce mémoire, les questions des pressions de sélection s'exerçant sur les performances d’alimentation par une tâche motrice nouvelle sont abordées afin de mieux comprendre l'évolution des capacités cognitives au sein d'une population captive de diamants mandarins (Taeniopygia guttata). Nous avons tout d'abord testé si les femelles diamants mandarins modifient leurs préférences d'accouplement après avoir observé la performance d'alimentation par une tâche motrice nouvelle des mâles. Afin de déterminer si les femelles sont capables de discriminer entre les mâles sur la base de leur capacité cognitive, nous avons également évalué les performances d’apprentissage de chacune d’elles. En effet, des études ont suggéré qu’il peut être coûteux, spécialement en terme de temps, de discriminer entre des partenaires potentiels sur cette base. La généralisation d’une préférence pour un mâle performant à d’autres mâles possédant le même phénotype permettrait la réduction de ces coûts. Nous avons donc finalement testé si les femelles diamants mandarins peuvent généraliser leur préférence après avoir observé les performances d’alimentation pour une tâche motrice nouvelle d’un mâle. Nos résultats suggèrent que les femelles diamants mandarins ne peuvent évaluer les capacités cognitives d’un mâle par l’intermédiaire de traits indicateurs. Toutefois, nous avons démontré qu’une observation directe des performances d’alimentation d’un mâle guide le choix d’appariement des femelles. Également, nous avons montré que les femelles peuvent généraliser l’apparence du mâle le plus performant et utiliser cette information lors de l’évaluation de nouveaux mâles. La relation entre les performances cognitives et le choix de partenaire pourraient s’expliquer par exemple par une meilleure exploitation de l’habitat, mais nécessite des études plus approfondies.

Female preference for male color is necessary and sufficient for assortative mating in 2 cichlid sister species

A critical step for speciation in the face of gene flow is the origination of reproductive isolation. The evolution of assortative mating greatly facilitates this process. Assortative mating can be mediated by one or multiple cues across an array of sensory modalities. We here explore possible cues that may underlie female mate choice in a sympatric species pair of cichlid fish from Lake Victoria, Pundamilia pundamilia and Pundamilia nyererei. Previous studies identified species-specific female preferences for male coloration, but effects of other cues could not be ruled out. Therefore, we assessed female choice in a series of experiments in which we manipulated visual (color) and chemical cues. We show that the visibility of differences in nuptial hue (i.e., either blue or red) between males of the 2 species is necessary and sufficient for assortative mating by female mate choice. Such assortment mediated by a single cue may evolve relatively quickly, but could make reproductive isolation vulnerable to environmental changes. These findings confirm the important role of female mate choice for male nuptial hue in promoting the explosive speciation of African haplochromine cichlids.

The mating system of the true fruit fly Bactrocera tryoniand its sister-species,Bactrocera neohumeralis

The frugivorous ‘true’ fruit fly, Bactrocera tryoni (Queensland fruit fly), is presumed to have a non-resourced-based lek mating system. This is largely untested, and contrary data exists to suggest Bactrocera tryoni may have a resource-based mating system focused on fruiting host plants. We tested the mating system of Bactrocera tryoni, and its close sibling Bactrocera neohumeralis, in large field cages using laboratory reared flies. We used observational experiments that allowed us to determine if: (i) mating pairs were aggregated or non-aggregated; (ii) mating system was resource or non-resource based; (iii) flies utilised possible landmarks (tall trees over short) as mate-rendezvous sites; and (iv) males called females from male-dominated leks. We recorded nearly 250 Bactrocera tryoni mating pairs across all experiments, revealing that: (i) mating pairs were aggregated; (ii) mating nearly always occurred in tall trees over short; (iii) mating was non-resource based; and (iv) that males and females arrived at the mate-rendezvous site together with no evidence that males preceded females. Bactrocera neohumeralis copulations were much more infrequent (only 30 mating pairs in total), but for those pairs there was a similar preference for tall trees and no evidence of a resource-based mating system. Some aspects of Bactrocera tryoni mating behaviour align with theoretical expectations of a lekking system, but others do not. Until evidence for unequivocal female choice can be provided (as predicted under a true lek), the mating system of Bactrocera tryoni is best described as a non-resource based, aggregation system for which we also have evidence that land-marking may be involved. This article is protected by copyright. All rights reserved

The mating system of the true fruit fly Bactrocera tryoni and its sister-species, Bactrocera neohumeralis

The frugivorous 'true' fruit fly, Bactrocera tryoni (Queensland fruit fly), is presumed to have a non-resourced-based lek mating system. This is largely untested, and contrary data exists to suggest Bactrocera tryoni may have a resource-based mating system focused on fruiting host plants. We tested the mating system of Bactrocera tryoni, and its close sibling Bactrocera neohumeralis, in large field cages using laboratory reared flies. We used observational experiments that allowed us to determine if: - (i) mating pairs were aggregated or non-aggregated; - (ii) mating system was resource or non-resource based; - (iii) flies utilised possible landmarks (tall trees over short) as mate-rendezvous sites, and; - (iv) males called females from male-dominated leks. We recorded nearly 250 Bactrocera tryoni mating pairs across all experiments, revealing that: - (i) mating pairs were aggregated; - (ii) mating nearly always occurred in tall trees over short; - (iii) mating was non-resource based, and; - (iv) that males and females arrived at the mate-rendezvous site together with no evidence that males preceded females. Bactrocera neohumeralis copulations were much more infrequent (only 30 mating pairs in total), but for those pairs there was a similar preference for tall trees and no evidence of a resource-based mating system. Some aspects of Bactrocera tryoni mating behaviour align with theoretical expectations of a lekking system, but others do not. Until evidence for unequivocal female choice can be provided (as predicted under a true lek), the mating system of Bactrocera tryoni is best described as a non-resource based, aggregation system for which we also have evidence that land-marking may be involved. This article is protected by copyright. All rights reserved.

Learning and natal host influence host preference, handling time and sex allocation behaviour in a pupal parasitoid

The host choice and sex allocation decisions of a foraging female parasitoid will have an enormous influence on the life-history characteristics of her offspring. The pteromalid Pachycrepoideus vindemiae is a generalist idiobiont pupal parasitoid of many species of cyclorrhaphous Diptera. Wasps reared in Musca domestica were larger, had higher attack rates and greater male mating success than those reared in Drosophila melanogaster. In no-choice situations, naive female R vindemiae took significantly less time to accept hosts conspecific with their natal host. Parasitoids that emerged from M. domestica pupae spent similar amounts of time ovipositing in both D. melanogaster and M. domestica. Those parasitoids that had emerged from D. melanogaster spent significantly longer attacking M. domestica pupae. The host choice behaviour of female P. vindemiae was influenced by an interaction between natal host and experience. Female R vindemiae reared in M. domestica only showed a preference among hosts when allowed to gain experience attacking M. domestica, preferentially attacking that species. Similarly, female parasitoids reared on D. melanogaster only showed a preference among hosts when allowed to gain experience attacking D. melanogaster, again preferentially attacking that species. Wasp natal host also influenced sex allocation behaviour. While wasps from both hosts oviposited more females in the larger host, M. domestica, wasps that emerged from M. domestica had significantly more male-biased offspring sex ratios. These results indicate the importance of learning and natal host size in determining R vindemiae attack rates. mating success, host preference and sex allocation behaviour, all critical components of parasitoid fitness.

Ornament colour selection, visual contrast and the shape of colour preference functions in great bowerbirds, Chlamydera nuchalis

A male bowerbird visual signal includes his own plumage, a structure he  constructs out of plant material and coloured objects (ornaments) he places on or near the structure to make up the bower. Plumage and bower together are used to attract females for mating. Ornaments are known to contrast with plumage, bower structure and visual backgrounds in seven Australian bowerbird species (Endler et al. 2005, Evolution, 50, 1795-1818). We estimated the colour preferences in a wild population of great bowerbirds using artificially coloured objects widely spaced in bird colour space. We found that these birds prefer colours that contrast with their own plumage, the bower structure and the visual backgrounds adjacent to the bower, and that they have very strong dislikes for colours that are similar to their own plumage and to the visual backgrounds. The range of disliked colour hues was much narrower than the range of preferred hues, suggesting that the word 'preference' may be misleading. Preferences for colour are inherently multidimensional and should be studied in the context of their function.

Environmental variation and the maintenance of polymorphism : the effect of ambient light spectrum on mating behaviour and sexual selection in guppies

The intensity of sexual selection is influenced by environmental conditions because these conditions influence signal propagation and the risks of the signal being exploited by predators and parasites. We explore the possibility that spatial or temporal heterogeneity in environmental signalling conditions (in this case light spectrum) may induce fluctuating sexual selection on male behaviour and ornamentation in guppies. We used shade cloth and filters to experimentally manipulate light spectrum, mimicking conditions found naturally: early morning/late afternoon light (SC treatment), midday forest shade (F89 filter treatment) and midday woodland shade (F55 filter treatment). Females were more responsive to male courtship and males were less likely to attempt sneak copulations under F55 light than the other two treatments. By contrast, male display rate was not influenced by treatment. Females tended to prefer the same males under SC and F55 light, but attractiveness in these treatments was unrelated to attractiveness under F89 light. There were similarities among treatments in the traits that females preferred: females preferred males with larger areas of orange in all three treatments. There were, however, also some differences, including preference for larger males under F89 light and for smaller males under the other treatments. Overall, the influence of ambient light spectrum on the relative importance of mate choice and male sneak copulation may have important implications for the mode and strength of sexual selection in different environments. The findings on attractiveness and preference functions, however, suggest that light spectrum only weakly affects the direction of sexual selection by female choice.

The effects of familiarity and group size on mating preferences in the guppy, Poecilia reticulata

In recent years, it has become evident that frequency dependence in the attractiveness of a particular phenotype to mates can contribute to the maintenance of polymorphism. However, these preferences for rare and unfamiliar male phenotypes have only been demonstrated in small, controlled experiments. Here, we tested the preference for unfamiliar mates in groups of six to 96 individuals over 13 days, in the guppy (Poecilia reticulata). We observed individual behaviour in situ to test whether fish discriminate two unfamiliar individuals among many familiar ones. We found that unfamiliar males and females were preferred over the familiar fishes in all groups and that this effect decayed over time. Increasing group sizes and levels of sexual activity did not hamper the preference for unfamiliar mates, providing further support for the role of frequency dependent mate choice in the maintenance of trait polymorphism in natural populations.

Assortative mating among animals of captive and wild origin following experimental conservation releases

Captive breeding is a high profile management tool used for conserving threatened species. However, the inevitable consequence of generations in captivity is broad scale and often-rapid phenotypic divergence between captive and wild individuals, through environmental differences and genetic processes. Although poorly understood, mate choice preference is one of the changes that may occur in captivity that could have important implications for the reintroduction success of captive-bred animals. We bred wild-caught house mice for three generations to examine mating patterns and reproductive outcomes when these animals were simultaneously released into multiple outdoor enclosures with wild conspecifics. At release, there were significant differences in phenotypic (e.g. body mass) and genetic measures (e.g. Gst and F) between captive-bred and wild adult mice. Furthermore, 83% of offspring produced post-release were of same source parentage, inferring pronounced assortative mating. Our findings suggest that captive breeding may affect mating preferences, with potentially adverse implications for the success of threatened species reintroduction programmes.

Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish

Rapid speciation in Lake Victoria cichlid fish of the genus Pundamilia may be facilitated by sexual selection: female mate choice exerts sexual selection on male nuptial coloration within species and maintains reproductive isolation between species. However, declining water transparency coincides with increasingly dull coloration and increasing hybridization. In the present study, we investigated the mechanism underlying this pattern in Pundamilia nyererei, a species that interbreeds with a sister species in turbid but not in clear water. We compared measures of intraspecific sexual selection between two populations from locations that differ in water transparency. First, in laboratory mate-choice experiments, conducted in clear water and under broad-spectrum illumination, we found that females originating from turbid water have significantly weaker preferences for male coloration than females originating from clear water. Second, both the hue and body coverage of male coloration differ between populations, which is consistent with adaptation to different photic habitats. These findings suggest that the observed relationship between male coloration and water transparency is not mediated by environmental variation alone. Rather, female mating preferences are indicated to have changed in response to this variation, constituting the first evidence for intraspecific preference-trait co-evolution in cichlid fish. (C) 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 398-406.

Assortative mating among Lake Malawi cichlid fish populations is not simply predictable from male nuptial colour

Background: Research on the evolution of reproductive isolation in African cichlid fishes has largely focussed on the role of male colours and female mate choice. Here, we tested predictions from the hypothesis that allopatric divergence in male colour is associated with corresponding divergence in preference. Methods: We studied four populations of the Lake Malawi Pseudotropheus zebra complex. We predicted that more distantly-related populations that independently evolved similar colours would interbreed freely while more closely-related populations with different colours mate assortatively. We used microsatellite genotypes or mesh false-floors to assign paternity. Fisher's exact tests as well as Binomial and Wilcoxon tests were used to detect if mating departed from random expectations. Results: Surprisingly, laboratory mate choice experiments revealed significant assortative mating not only between population pairs with differently coloured males, but between population pairs with similarly-coloured males too. This suggested that assortative mating could be based on nonvisual cues, so we further examined the sensory basis of assortative mating between two populations with different male colour. Conducting trials under monochromatic (orange) light, intended to mask the distinctive male dorsal fin hues (blue v orange) of these populations, did not significantly affect the assortative mating by female P. emmiltos observed under control conditions. By contrast, assortative mating broke down when direct contact between female and male was prevented. Conclusion: We suggest that non-visual cues, such as olfactory signals, may play an important role in mate choice and behavioural isolation in these and perhaps other African cichlid fish. Future speciation models aimed at explaining African cichlid radiations may therefore consider incorporating such mating cues in mate choice scenarios.

Hotshots, hot spots, and female preference: exploring lek formation models with a bower-building cichlid fish

In many animals, males congregate in leks that females visit for the sole purpose of mating. We observed male and female behavior on 3 different-sized leks of the bower-building cichlid fish Nyassachromis cf. microcephalus to test predictions of 3 prominent lek models: the "hotshot," "hot spot," and "female preference" models. In this system, we were able to refine these predictions by distinguishing between indirect mate choice, by which females restrict their set of potential mates in the absence of individual male assessment, and direct mate choice, by which females assess males and their territories through dyadic behavioral interactions. On no lek were males holding central territories favored by indirect or direct mate choice, contrary to the prediction of the hotshot model that leks form because inferior males establish territories surrounding hotshot males preferred by females. Average female encounter rate of males increased with lek size, a pattern typically interpreted as evidence that leks form through female preference for lekking males, rather than because males congregate in hot spots of high female density. Female propensity to engage in premating behavior once courted did not increase with lek size, suggesting female preference for males on larger leks operated through indirect choice rather than direct choice based on individual assessment. The frequency of male-male competitive interactions increased with lek size, whereas their foraging rate decreased, implying a cost to males maintaining territories on larger leks. Together these data most strongly support the female preference model, where females may benefit through indirect mate choice for males able to meet the competitive cost of occupying larger leks.

Tracing reinforcement through asymmetrical partner preference in the European common vole Microtus arvalis

Background The mechanistic basis of speciation and in particular the contribution of behaviour to the completion of the speciation process is often contentious. Contact zones between related taxa provide a situation where selection against hybridization might reinforce separation by behavioural mechanisms, which could ultimately fully isolate the taxa. One of the most abundant European mammals, the common vole Microtus arvalis, forms multiple natural hybrid zones where rapidly diverging evolutionary lineages meet in secondary contact. Very narrow zones of hybridization spanning only a few kilometres and sex-specific gene flow patterns indicate reduced fitness of natural hybrids and incipient speciation between some of the evolutionary lineages. In this study, we examined the contribution of behavioural mechanisms to the speciation process in these rodents by fine-mapping allopatric and parapatric populations in the hybrid zone between the Western and Central lineages and experimental testing of the partner preferences of wild, pure-bred and hybrid female common voles. Results Genetic analysis based on microsatellite markers revealed the presence of multiple parapatric and largely non-admixed populations at distances of about 10 km at the edge of the area of natural hybridization between the Western and Central lineages. Wild females from Western parapatric populations and lab-born F1 hybrids preferred males from the Western lineage whereas wild females of Central parapatric origin showed no measurable preference. Furthermore, wild and lab-born females from allopatric populations of the Western or Central lineages showed no detectable preference for males from either lineage. Conclusions The detected partner preferences are consistent with asymmetrical reinforcement of pre-mating reproductive isolation mechanisms in the European common vole and with earlier results suggesting that hybridization is more detrimental to the Western lineage. As a consequence, these differences in behaviour might contribute to a further geographical stabilization of this moving hybrid zone. Such behavioural processes could also provide a mechanistic perspective for frequently-detected asymmetrical introgression patterns in the largely allopatrically diversifying Microtus genus and other rapidly speciating rodents.