Genetic and environmental effects on the covariation betweencolour polymorphism and a life history trait

Variation in coloration with a strong underlying genetic basis is frequently found within animal populations but little is known about its function. Covariation between colour polymorphism and life-history traits can arise because morphs perform differently among environments or because they possess alternative alleles coding for key life-history traits. To test these two hypotheses, we studied a population of tawny owls Strix aluco, a bird displaying red, brown and grey morphs. We assessed the colour morph of breeding females, swapped eggs or hatchlings between pairs of nests, and examined how body condition in 3-week-old nestlings covaries with coloration of foster and genetic mothers. Redder foster and genetic mothers produced young in better condition. Because in two other years we observed that greyish females produced offspring in better condition than those of red females, the present study suggests that colour polymorphism signals genetic and phenotypic adaptations to cope with a fluctuating environment.

Sexual selection in genetic colour-polymorphic species: a review of experimental studies and perspectives

Sexual selection theory has primarily focussed on the role of mating preferences for the best individuals in the evolution of condition-dependent ornaments, traits that signal absolute quality. Because the most suitable mate for one individual is not always the best for others, however, we argue that non-directional mate choice can promote the evolution of alternative morphs that are not condition-dependent in their expression (i.e. genetic polymorphism). We list the different mate-choice rules (i.e. all individuals have the same preference; preference depends on the chooser's morph; individuals mate preferentially with conspecifics displaying an uncommon or the most frequent morph) and review experimental studies that investigated mate choice in natural populations of colour-polymorphic animals. Our review emphasises that although the experimental data support the idea that sexual selection plays an important role in the evolution of genetic colour polymorphism in many different ways, little is known about the adaptive value of each mate-choice strategy and about their implication in the evolutionary stability of colour polymorphism. One way of solving this problem is to determine the adaptive function of colour morphs, a worthwhile objective, because better understanding of mate-choice rules in polymorphic species should provide important insights into sexual-selection processes and, in turn, into the maintenance of genetic variation.

Natural selection in a postglacial range expansion: the case of the colour cline in the European barn owl.

Gradients of variation-or clines-have always intrigued biologists. Classically, they have been interpreted as the outcomes of antagonistic interactions between selection and gene flow. Alternatively, clines may also establish neutrally with isolation by distance (IBD) or secondary contact between previously isolated populations. The relative importance of natural selection and these two neutral processes in the establishment of clinal variation can be tested by comparing genetic differentiation at neutral genetic markers and at the studied trait. A third neutral process, surfing of a newly arisen mutation during the colonization of a new habitat, is more difficult to test. Here, we designed a spatially explicit approximate Bayesian computation (ABC) simulation framework to evaluate whether the strong cline in the genetically based reddish coloration observed in the European barn owl (Tyto alba) arose as a by-product of a range expansion or whether selection has to be invoked to explain this colour cline, for which we have previously ruled out the actions of IBD or secondary contact. Using ABC simulations and genetic data on 390 individuals from 20 locations genotyped at 22 microsatellites loci, we first determined how barn owls colonized Europe after the last glaciation. Using these results in new simulations on the evolution of the colour phenotype, and assuming various genetic architectures for the colour trait, we demonstrate that the observed colour cline cannot be due to the surfing of a neutral mutation. Taking advantage of spatially explicit ABC, which proved to be a powerful method to disentangle the respective roles of selection and drift in range expansions, we conclude that the formation of the colour cline observed in the barn owl must be due to natural selection.

Evolutionary ecology of the colour-dimorphic rewardless orchid "Dactylorhiza sambucina"

Abstract Phenotypic polymorphism is an ideal system to study natural selection in wild populations, because it allows tracking population genetic changes by means of phenotypic changes. A wide variety of polymorphic traits have been studied in numerous animals and plants, as for example colour patterns in moths, snails and birds, human laterality, male reproductive strategies, plant morphology or mating systems. This thesis focused on Dactylorhiza sarnbucina, a rewardless European orchid species, showing a striking flower colour polymorphism, with either yellow or red flowered individuals co-occurring in natural populations. Several studies have investigated its evolutionary ecology since Nilsson's seminal paper in 1980, with a particular emphasis in the evolution and maintenance of its colour polymorphism. One of the main selective forces proposed to maintain this colour polymorphism was pollinator driven negative frequency-dependent selection (NFDS), when each morph is advantaged when rare, and comparatively disadvantaged when common. However, other investigators have recently questioned the occurrence of NFDS, and proposed alternatively that fluctuating selection may maintain this colour polymorphism. In this thesis, we aimed at reviewing and synthesizing these different studies, and also brought our contribution on D. sambucina reproductive ecology. Because numerous hypotheses have still to be tested, we concluded by saying that we are a long way from understanding the evolution and dynamics of colour polymorphism in natural D. sambucina populations. Beside the debated question of colour polymorphism maintenance, one question remained to be tested: what are the consequences of polymorphism per se. We experimentally addressed this question using artificial populations of D. sambucina, and found no relationship between population phenotypic diversity and orchid pollination success. This finding suggest that polymorphism itself was not an advantage for deceptive species such D sambucina, contrarily to the expectations. Finally, we suggest potential research perspectives that could allow a better understanding of the evolutionary ecology of this species. Résumé Le polymorphisme phénotypique est un système biologique idéal pour étudier l'action de la sélection en populations naturelles, grâce à la possibilité de suivre les changements génétiques de la population en étudiant les phénotypes des individus. De très nombreuses études ont montré du polymorphisme phénotypique chez les animaux, par exemple la latéralité chez l'Homme, la coloration des escargots ou des oiseaux. Dans le règne végétal, le polymorphisme est souvent associé à des traits du système de reproduction. Cette thèse est centrée sur une espèce d'orchidée Européenne qui ne produit pas de nectar, Dactylorhiza sambucina. Cette espèce présente des individus à fleurs jaunes et des individus à fleurs rouge, généralement présents en mélange dans les populations naturelles. Plusieurs études ont investigué l'écologie évolutive de cette espèce depuis 25 ans, avec comme thème central l'évolution et le maintien de ce polymorphisme. La principale force sélective proposée pour maintenir ce polymorphisme de couleur est la sélection fréquence-dépendante, exercée par le comportement des pollinisateurs. Chacun des deux variants de couleur est favorisé quand il est rare, et défavorisé quand il devient commun. Bien que ce mécanisme semble agir, certains auteurs doutent de son importance, et ont proposé que les variations temporelles ou spatiales des forces de sélection puisse maintenir le polymorphisme de couleur chez D. sambucina. Dans cette thèse, nous avons voulu résumer et synthétiser les résultats de ces différentes études, et aussi présenter des données nouvelles concernant la reproduction de cette espèce. À la vue de ces résultats, il apparait que de nombreux points nécessitent des expériences complémentaires, et que la compréhension de ce système biologique est encore fragmentaire. Nous nous sommes également intéressés à une question laissée en suspens dans la littérature: le polymorphisme de couleur en soit confère-t-il un avantage à l'espèce, comme proposé par certains auteurs? En construisant des populations artificielles de D. sambucina, nous avons pu montrer que le polymorphisme de couleur n'augmente pas le succès reproducteur de l'espèce. Nous terminons ce travail de recherche en proposant plusieurs axes de recherche pouvant conduire à une meilleure compréhension de l'écologie et de l'évolution de cette espèce.

Sympatric colour polymorphisms associated with nonrandom gene flow in cichlid fish of Lake Victoria

Colour polymorphisms have fascinated evolutionary ecologists for a long time. Yet, knowledge on the mechanisms that allow their persistence is restricted to a handful of well-studied cases. We studied two species of Lake Victoria cichlid fish, Neochromis omnicaeruleus and Neochromis greenwoodi, exhibiting very similar sex-linked colour polymorphisms. The ecology and behaviour of one of these species is well studied, with colour-based mating and aggression preferences. Here, we ask whether the selection potentially resulting from female and male mating preferences and aggression biases reduces gene flow between the colour morphs and permits differentiation in traits other than colour. Over the past 14 years, the frequencies of colour morphs have somewhat oscillated, but there is no evidence for directional change, suggesting the colour polymorphism is persistent on an ecological timescale. We find limited evidence of ecomorphological differentiation between sympatric ancestral (plain) and derived (blotched) colour morphs. We also find significantly nonrandom genotypic assignment and an excess of linkage disequilibrium in the plain morph, which together with previous information on mating preferences suggests nonrandom mating between colour morphs. This, together with negative frequency-dependent sexual selection, found in previous studies, may facilitate maintenance of these polymorphisms in sympatry

Positive effect of the yellow morph on female reproductive success in the flower colour polymorphic Iris lutescens (Iridaceae), a deceptive species

The deceptive Iris lutescens (Iridaceae) shows a heritable and striking flower colour polymorphism, with both yellow- and purple-flowered individuals growing sympatrically. Deceptive species with flower colour polymorphism are mainly described in the family Orchidaceae and rarely found in other families. To explain the maintenance of flower colour polymorphism in I.lutescens, we investigated female reproductive success in natural populations of southern France, at both population and local scales (within populations). Female reproductive success was positively correlated with yellow morph frequency, at both the population scale and the local scale. Therefore, we failed to observe negative frequency-dependent selection (NFDS), a mechanism commonly invoked to explain flower colour polymorphism in deceptive plant species. Flower size and local flower density could also affect female reproductive success in natural populations. Pollinator behaviour could explain the positive effect of the yellow morph, and our results suggest that flower colour polymorphism might not persist in I.lutescens, but alternative explanations not linked to pollinator behaviour are discussed. In particular, NFDS, although an appealingly simple explanation previously demonstrated in orchids, may not always contribute to maintaining flower colour polymorphism, even in deceptive species.

Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection

We investigated a Lake Victoria cichlid with a complex colour polymorphism that apparently represents one original species and two incipient species, all of which are sympatric. In laboratory breeding experiments we observed sex ratio distortion in certain matings between original and incipient species. Mate choice experiments show that males of the incipient species exhibit mating preferences against the original species, and males and females of the original species exhibit strong mating preferences against the incipient species. Mating preferences might evolve by sex ratio selection to avoid matings with distorted progeny sex ratios. Phenotype frequencies in nature suggest that mating preferences translate into mating frequencies, thus restricting gene flow and exerting disruptive sexual selection between the original and incipient species. The incipient species do not differ in morphology or ecology from the original species, implying that colour polymorphism, associated with sex ratio distortion, can be an incipient stage in sympatric speciation, and that disruption of gene flow can precede ecological differentiation

Can ancient colour polymorphisms explain why some cichlid lineages speciate rapidly under disruptive sexual selection?

It is not sufficiently understood why some lineages of cichlid fishes have proliferated in the Great Lakes of East Africa much more than anywhere else in the world, and much faster than other cichlid lineages or any other group of freshwater fish. Recent field and experimental work on Lake Victoria haplochromines suggests that mate choice-mediated disruptive sexual selection on coloration, that can cause speciation even in the absence of geographical isolation, may explain it. We summarize the evidence and propose a hypothesis for the genetics of coloration that may help understand the phenomenon. By detl ning colour patterns by hue and arrangement of hues on the body, we could assign almost all observed phenotypes of Lake Victoria cichlids to one of three female («plain», «orange blotched», «black and white») and three male («blue», «red-ventrum», «reddorsum») colour patterns. These patterns diagnose species but frequently eo-occur also as morphs within the same population, where they are associated with variation in mate preferences, and appear to be transient stages in speciation. Particularly the male patterns occur in almost every genus of the species flock. We propose that the patterns and their association into polymorphisms express an ancestral trait that is retained across speciation. Our model for male colour pattern assumes two structural loci. When both are switched off, the body is blue. When switched on by a cascade of polymorphic regulatory genes, one expresses a yellow to red ventrum, the other one a yellow to red dorsum. The expression of colour variation initiates speciation. The blue daughter species will inherit the variation at the regulatory genes that can, without new mutational events, purely by recombination, again expose the colour polymorphism, starting the process anew. Very similar colour patterns also dominate among the Mbuna of Lake Malawi. In contrast, similar colour polymorphisms do not exist in the lineages that have not proliferated in the Great Lakes. The colour pattern polymorphism may be an ancient trait in the lineage (or lineages) that gave rise to the two large haplochromine radiations. We propose two tests of our hypothesis.

Metabolism, oxidative stress and territorial behaviour in a female colour polymorphic cichlid fish

Intrasexual selection on body coloration is thought to play an important role in the evolution of colour polymorphism, but its physiological underpinnings have received limited attention. In the colour polymorphic cichlid Neochromis omnicaeruleus, three fully sympatric female colour morphs— a plain morph (P) and two conspicuously coloured blotched morphs, black-and-white blotched (WB) and orange blotched (OB)—differ in agonistic behaviour. We compared routine metabolic rate (when females were housed in social isolation), short-term energetic costs of interacting with a same-colour rival housed in an adjacent transparent chamber and oxidative stress between the three female colour morphs. WB females had a lower routine metabolic rate compared with the other colour morphs. WB females also had a lower active metabolic rate during inter-female interactions than OB females, while OB females used more oxygen per unit aggressive act than the other two colour morphs. However, there were no consistent differences in oxidative stress between the three morphs. Concerted divergence in colour, behaviour and metabolism might contribute to the evolution of these polymorphisms in sympatry.

Local adaptation and matching habitat choice in female barn owls with respect to melanic coloration.

Local adaptation is a major mechanism underlying the maintenance of phenotypic variation in spatially heterogeneous environments. In the barn owl (Tyto alba), dark and pale reddish-pheomelanic individuals are adapted to conditions prevailing in northern and southern Europe, respectively. Using a long-term dataset from Central Europe, we report results consistent with the hypothesis that the different pheomelanic phenotypes are adapted to specific local conditions in females, but not in males. Compared to whitish females, reddish females bred in sites surrounded by more arable fields and less forests. Colour-dependent habitat choice was apparently beneficial. First, whitish females produced more fledglings when breeding in wooded areas, whereas reddish females when breeding in sites with more arable fields. Second, cross-fostering experiments showed that female nestlings grew wings more rapidly when both their foster and biological mothers were of similar colour. The latter result suggests that mothers should particularly produce daughters in environments that best match their own coloration. Accordingly, whiter females produced fewer daughters in territories with more arable fields. In conclusion, females displaying alternative melanic phenotypes bred in habitats providing them with the highest fitness benefits. Although small in magnitude, matching habitat selection and local adaptation may help maintain variation in pheomelanin coloration in the barn owl.

Ultraviolet reflectance in a melanin-based plumage trait is heritable

Question: Is ultraviolet (UV) reflectance of melanin-based plumage ornaments heritable? Data studied: We considered the barn owl (Two alba), a species that varies continuously from white to reddish-brown, a pheomelanin-based trait. Methods: To perform a partial cross-fostering experiment. we exchanged one to three hatchlings between 16 pairs of nests with a similar hatching date. This experiment allocated hatchlings randomly among rearing environments. Forty-nine days later, we collected three feathers per individual to measure UV reflectance. Conclusions: The cross-fostering experiment showed that. independently of human-visible coloration, variation in UV reflectance is significantly sensitive to origin-related factors.

Melanism, body condition and elevational distribution in the asp viper

Alternative morphotypes can confer important selective advantages in different habitats, whereas they can be penalized in other circumstances. In ectotherms, such as reptiles, the body colour can have direct effects on numerous aspects of their existence, such as thermoregulation or prey-predator interactions. Darker melanic individuals show lower skin reflectance and consequently heat up more rapidly and maintain optimal body temperatures more easily than lighter coloured individuals. As a consequence, melanistic individuals of diurnal species in cool areas may exhibit higher body condition, growth rate, survival and fecundity than lighter coloured individuals. Such advantages of dark coloration may be counterbalanced by a lower crypsis to predators and a decreased foraging efficiency. We investigated, in two montane populations of asp vipers Vipera aspis, the relationship between (1) colour polymorphism and body condition and length and (2) the coloration of individuals and their elevational distribution. We showed significant relationships between (1) the coloration, body condition and sex of individuals; (2) sexes and reproductive state and morph frequency; and (3) colour morphs that were distributed following an elevational gradient. Hence, colour polymorphism plays an important role in the ecology and evolution of the asp viper and is maintained through differential selective pressures.

Personality and melanin-based colouration traits in barn owls, tawny owl and kestrels

Individuals need to adapt to their local environment in order to survive. When selection pressures differ in local populations, polymorphism can evolve. Colour polymorphism is one of the most obvious polymorphisms since it is readily observable. Different sources of colouration exist, but melanin-based colouration is one of the most common in birds. The melanocortin system produces this colouration and because the melanocortin system has pleiotropic effects on behavioural and physiological traits, it is a good candidate to be an underlying mechanism to explain the maintenance of colour polymorphism. In this thesis I studied three different raptors which all display melanin-based colouration; barn owls (Tyto alba), tawny owls (Strix aluco) and Eurasian kestrels (Falco tinnunculus). The main question was if there was a relationship between melanin-based colouration and individual behavioural differences. The underlying hypothesis is that colour could be a signal of certain adaptive traits. Our goal was to find evolutionary explanations for the persistence of colour polymorphism. I found that nestling kestrels and barn owls differ in anti-predatory behaviour, with respect to their melanic colouration (chapters 1 and 2). Darker individuals show less reaction to human handling, but in kestrels aggression and colouration are related in opposite ways than in barn owls. More reddish barn owls travel greater distances in natal dispersal and this behaviour is repeatable between parents and same sex offspring (chapter 3). Dark reddish tawny owls defend their nests more intensely against intruders and appear to suffer less from nest predation (chapter 4). Finally I show that polymorphism in the Melanocortin 1 receptor gene (MC1R), which is strongly correlated with reddish colouration in the barn owl, is related to natal dispersal distance, providing a first indication for a genetic basis of the relation between this behaviour and colouration (chapter 5). My results demonstrate a clear link between melanin-based colouration and animal personality traits. I demonstrated this relation in three different species, which shows there is most likely a general underlying mechanism responsible. Different predation pressures might have shaped the reactions to predation, but also differences in sex-related colouration. Male-like and female-like colouration might signal more or less aggressive behaviour. Fluctuating environmental conditions might cause different individual strategies to produce equal reproductive success. The melanocortin system with its pleiotropic effects might be an underlying mechanism, as suggested by the results from the genetic polymorphism, the similar results found in these three species and by the similar relations reported in other species. This thesis demonstrates that colouration and individual differences are correlated and it provides the first glimpse of an underlying system. We can now conduct a more directed search for underlying mechanisms and evolutionary explanations with the use of quantitative genetic methods.

Similar patterns of local barn owl adaptation in the Middle East and Europe with respect to melanic coloration

The maintenance of phenotypic variation is a central question in evolutionary biology. A commonly suggested mechanism is that of local adaptation, whereby different phenotypes are adapted to alternative environmental conditions. A recent study in the European barn owl (Tyto alba) has shown that natural selection maintains a strong clinal variation in reddish pheomelanin-based coloration. Studies in the region where phenotypic variation in this owl is the highest in Europe have further demonstrated that dark-reddish and pale-reddish owls exploit open and wooded habitats, predate voles and wood mice, and are long-tailed and short-tailed, respectively. However, it remains unclear as to whether these traits evolved as a consequence of allopatric evolution of dark colour in northern Europe and white colour in southern Europe, during which owls could have also evolved different morphologies and foraging behaviour. This scenario implies that covariation between coloration and foraging behaviour could be a specificity of the European continent, which is not found in other worldwide-distributed populations. To investigate this issue we studied a barn owl population in the Middle East. Our results show that, as in Central Europe, dark-reddish female owls breed more often in the open landscape than their pale-reddish female conspecifics, their offspring are fed with more voles than Muridae, and they are longer-winged and longer-tailed. These findings indicate that in the barn owl the association in females between pheomelanin-based coloration and foraging behaviour and morphology is not restricted to the European continent but may well evolve in sympatry in many barn owl populations worldwide.

Pheomelanin-based colouration is correlated with indices of flying strategies in the barn owl

Resource polymorphism refers to individuals from the same population foraging in alternative habitats or on alternative food. Food specialization can be associated with adaptations such as colour polymorphism, with pale and dark colours conferring differential camouflage in different habitats. Pale and dark-reddish pheomelanic Barn Owls (Tyto alba) forage on different prey species in closed and open habitats, respectively. We show here that darker-reddish owls have heavier stomach content when found dead, and their 5th secondary wing feather is more deeply anchored inside the integument. These correlations suggest that their feathers bend less when flying, and that darker-reddish Barn Owls are able sustain more intense flying than their paler conspecifics.