Demographic history, genetic structure and gene flow in a steppe-associated raptor species

<p>Abstract</p> <p>Background</p> <p>Environmental preferences and past climatic changes may determine the length of time during which a species range has contracted or expanded from refugia, thereby influencing levels of genetic diversification. Connectivity among populations of steppe-associated taxa might have been maximal during the long glacial periods, and interrupted only during the shorter interglacial phases, potentially resulting in low levels of genetic differentiation among populations. We investigated this hypothesis by exploring patterns of genetic diversity, past demography and gene flow in a raptor species characteristic of steppes, the Montagu's harrier (<it>Circus pygargus</it>), using mitochondrial DNA data from 13 breeding populations and two wintering populations.</p> <p>Results</p> <p>Consistent with our hypothesis, Montagu's harrier has relatively low genetic variation at the mitochondrial DNA. The highest levels of genetic diversity were found in coastal Spain, France and central Asia. These areas, which were open landscapes during the Holocene, may have acted as refugia when most of the European continent was covered by forests. We found significant genetic differentiation between two population groups, at the SW and NE parts of the species' range. Two events of past population growth were detected, and occurred ca. 7500-5500 and ca. 3500-1000 years BP in the SW and NE part of the range respectively. These events were likely associated with vegetation shifts caused by climate and human-induced changes during the Holocene.</p> <p>Conclusions</p> <p>The relative genetic homogeneity observed across populations of this steppe raptor may be explained by a short isolation time, relatively recent population expansions and a relaxed philopatry. We highlight the importance of considering the consequence of isolation and colonization processes in order to better understand the evolutionary history of steppe species.</p

FONCTIONS ADAPTATIVES DES SIGNAUX COLORES CHEZ LES RAPACES. Cas des traits colorés à base de caroténoïdes, d'ultraviolet et de mélanine chez deux espèces de Busard, le Busard des roseaux Circus aeruginosus et le Busard cendré C. pygargus

Within the framework of this thesis, I was interested in raptors' colored traits. More precisely, I tried to understand the potential functions associated with two types of coloured traits widely encountered in raptors, carotenoids-based (and which reflect in the ultraviolet), and melanin-based traits. I chose to study two close-related species of harriers, the Marsh (Circus aeruginosus) and the Montagu's Harrier (Circus pygargus), and I employed both empirical and experimental methods. Firstly, I assessed the origin and the maintenance of the plumage polymorphism existing within a population of Marsh Harrier. I described as precisely as possible the colour variations within this polymorphism, and then, I explored potential adaptive advantages according to different morphs expressed, and especially in males. I focused my research on the foraging efficiency, social dominancy and access to mate. Briefly, the plumage polymorphism existing within this population seems to be due to a very high density that would have generated the apparition of two alternative behavioural strategies within the gender male. The first one concerned males expressing a 'grey' morph, which was the most widespread in low density populations and which was related to solitary and territorial behaviour. The second one was related to the apparition of a 'dark' morph, femalelike, for which males would be much more social, and would profit from the imitation of female's plumage, through conflict's reduction with 'grey' males. In addition, I also studied the potential functions of this polymorphism during a particular type of social relations existing in harriers, the group defence or 'mobbing'. I detected individual 'roles' within a typical sequence of mobbing, roles that are partially defined by individual morphs. Secondly, I analyzed the mechanisms of carotenoid-based traits' development, and I tested a potential function associated to the expression of those traits in harriers' chicks. More especially, I showed that harriers' nestlings express carotenoid-based traits early in life, but that they are limited for the access of carotenoids, primarily through the abundance of their principal preyspecies, the common Vole. In addition, it appears that carotenoid-based traits of harriers' nestlings would be implied in the parent-offspring communication, and in particular, that the modification of their colour, either within ultraviolets or in yellow color. I involved consequences in term of parent feeding behaviour. The potential function associated with carotenoid-based traits of harrier nestlings, such as for example, within brood-communication framework, still remains to be accurately investigated.Dans le cadre de cette thèse, je me suis intéressée aux traits colorés chez les rapaces. Plus particulièrement, j'ai tenté de comprendre les fonctions potentielles associées à deux types de traits colorés chez les rapaces, les traits à base de caroténoïdes (et qui reflètent dans les ultraviolets), et les traits à base de mélanine, à travers l'étude du polymorphisme de plumage. Pour ce faire, j'ai choisi d'étudier deux espèces proches de busards, le Busard des roseaux Circus aeruginosus et le Busard cendré Circus pygargus et j'ai employé des méthodes à la fois empirique et expérimentale. Dans un premier temps, j'ai tenté de comprendre l'origine et le maintien du polymorphisme de plumage existant au sein d'une population de Busard des roseaux, en tentant d'une part de décrire précisément les variations de coloration au sein de ce polymorphisme, et en m'intéressant d'autre part à l'existence d'éventuels avantages adaptatifs selon les différents morphes exprimés chez les individus, et en particulier les mâles, en terme d'accès aux ressources alimentaires, de dominance sociale et d'accès aux partenaires de reproduction. Très brièvement, le polymorphisme de plumage existant au sein de cette population semble être du à une très forte densité, qui aurait engendrée l'apparition de deux stratégies comportementales alternatives au sein du sexe mâle, la première étant la plus répandue dans les populations à faible densité et concernant des mâles exprimant un morphe 'gris', à tendance solitaire et territoriale, et la seconde concernant l'apparition d'un morphe 'sombre', de type femelle, pour lequel les mâles seraient beaucoup plus sociaux, et bénéficierait de l'imitation du plumage des femelles à travers la réduction des conflits avec les mâles 'gris'. Par ailleurs, j'ai également étudié les fonctions potentielles de ce polymorphisme au cours d'un type particulier de relations sociales existant chez les busards, la défense de groupe ou « mobbing ». Il apparaît des 'rôles' au sein d'une séquence de défense de groupe classique définis entre autre par les morphes exprimés par les individus. Dans un deuxième temps, j'ai analysé les mécanismes de développement, et j'ai testé une fonction potentielle associée à l'expression des traits à base de caroténoïdes chez les poussins de busards. Plus particulièrement, j'ai démontré que les jeunes busards expriment des traits à base de caroténoïdes dès leur plus jeune âge, mais qu'ils sont limités, en condition naturelle, pour l'accès aux caroténoïdes, et ce, essentiellement à travers l'abondance de leur espèce-proie principale, le campagnol. Par ailleurs, il semble apparaître que les traits colorés des jeunes busards seraient impliqués dans la communication parents-enfants, et plus particulièrement, que la modification de leur coloration, au niveau des ultraviolets ou du 'jaune' (i.e. caroténoïdes), entraîne des conséquences en terme de nourrissage, de la part de leurs parents. Il reste cependant encore à analyser plus en détail la fonction associé aux traits colorés chez les jeunes busards, comme par exemple au niveau de la communication entre jeunes d'une même nichée

Comparative breeding performance of Marsh Harriers Circus aeruginosus along a gradient of land-use intensification and implications for population management

Assessing variation in breeding performance in relation to habitat characteristics may provide insights into predicting the consequences of land-use change on species ecology and population dynamics. We compared four Marsh Harrier Circus aeruginosus populations subject to similar environmental conditions, but which differed in habitat composition, ranging from natural habitats to intensively cultivated areas. Using a 6-year dataset, we characterized breeding habitat and diet in these four study sites, and analysed breeding performance in relation to this gradient of land-use intensification. There was minimal variation in breeding performance between study years but consistent variation between study sites. Unexpectedly, Marsh Harriers breeding in intensively cultivated habitats had higher reproductive success than those breeding in more natural habitats, which, however, hosted higher breeding densities, so overall net population productivity (fledglings per unit area) was similar across sites. This resulted from combined effects of density-dependence and different predation rates between study sites. The colonization of intensive farmland habitats may not necessarily impact negatively on population sustainability when breeding success and population density are traded against each other. However, our findings should not mask longer-term conservation issues for populations breeding in these intensively managed areas, and further studies should assess potential long-term negative effects of occupancy of human-altered habitat.This study was conducted under a licence granted by the CRBPO (Muséum National d’Histoire Naturelle). Part of this research was funded by DREAL Poitou-Cha-rentes, ANR-BIODIVAGRIM and ANR-ERANET Eco-cycles.Peer Reviewe

Fonctions adaptatives des signaux colorés chez les rapaces (cas des traits colorés à base de caroténoïdes, d'ultraviolet et de mélanine chez deux espèces de Busard, le Busard des roseaux Circus aeruginosus et le Busard cendré C. pygargus)

Dans le cadre de cette thèse, je me suis intéressée aux traits colorés chez les rapaces. Plus particulièrement, j ai tenté de comprendre les fonctions potentielles associées à deux types de traits colorés chez les rapaces, les traits à base de caroténoïdes (et qui reflètent dans les ultraviolets), et les traits à base de mélanine, à travers l étude du polymorphisme de plumage. Pour ce faire, j ai choisi d étudier deux espèces proches de busards, le Busard des roseaux Circus aeruginosus et le Busard cendré Circus pygargus et j ai employé des méthodes à la fois empirique et expérimentale. Dans un premier temps, j ai tenté de comprendre l origine et le maintien du polymorphisme de plumage existant au sein d une population de Busard des roseaux, en tentant d une part de décrire précisément les variations de coloration au sein de ce polymorphisme, et en m intéressant d autre part à l existence d éventuels avantages adaptatifs selon les différents morphes exprimés chez les individus, et en particulier les mâles, en terme d accès aux ressources alimentaires, de dominance sociale et d accès aux partenaires de reproduction. Très brièvement, le polymorphisme de plumage existant au sein de cette population semble être du à une très forte densité, qui aurait engendrée l apparition de deux stratégies comportementales alternatives au sein du sexe mâle, la première étant la plus répandue dans les populations à faible densité et concernant des mâles exprimant un morphe gris , à tendance solitaire et territoriale, et la seconde concernant l apparition d un morphe sombre , de type femelle, pour lequel les mâles seraient beaucoup plus sociaux, et bénéficierait de l imitation du plumage des femelles à travers la réduction des conflits avec les mâles gris . Par ailleurs, j ai également étudié les fonctions potentielles de ce polymorphisme au cours d un type particulier de relations sociales existant chez les busards, la défense de groupe ou mobbing . Il apparaît des rôles au sein d une séquence de défense de groupe classique définis entre autre par les morphes exprimés par les individus. Dans un deuxième temps, j ai analysé les mécanismes de développement, et j ai testé une fonction potentielle associée à l expression des traits à base de caroténoïdes chez les poussins de busards. Plus particulièrement, j ai démontré que les jeunes busards expriment des traits à base de caroténoïdes dès leur plus jeune âge, mais qu ils sont limités, en condition naturelle, pour l accès aux caroténoïdes, et ce, essentiellement à travers l abondance de leur espèce-proie principale, le campagnol. Par ailleurs, il semble apparaître que les traits colorés des jeunes busards seraient impliqués dans la communication parents-enfants, et plus particulièrement, que la modification de leur coloration, au niveau des ultraviolets ou du jaune (i.e. caroténoïdes), entraîne des conséquences en terme de nourrissage, de la part de leurs parents. Il reste cependant encore à analyser plus en détail la fonction associé aux traits colorés chez les jeunes busards, comme par exemple au niveau de la communication entre jeunes d une même nichée.PARIS-BIUSJ-Thèses (751052125) / SudocPARIS-BIUSJ-Physique recherche (751052113) / SudocSudocFranceF

Carotenoid limitation and allocation priorities in asynchronous raptor nestlings

The evolution and maintenance of conspicuous animal traits and communication signals have long fascinated biologists. Many yellow-red conspicuous traits are coloured by carotenoid pigments, and in some species they are displayed at a very young age. In nestling birds, the functions and proximate mechanisms of carotenoid-pigmented traits are probably different and not as well known as those of adults. Here we investigated how Montagu's harrier (Circus pygargus) nestlings within structured families used a limited resource, carotenoid pigments, and whether they used these for increasing coloration (deposition in integuments) or for mounting a response to a phytohaemagglutinin (PHA) challenge, which measures pro-inflammatory potential and aspects of cellular immune responsiveness. We manipulated carotenoid availability, using dietary carotenoid supplementations, and show that when supplemented, nestlings primarily allocated supplemental carotenoids to increase their coloration, irrespective of their sex, but depending of their position within the brood. Responses to PHA challenge were condition-dependent, but depending on carotenoid availability. Moreover, how nestlings allocated carotenoids depended on their rank within the brood, which in turn influenced their level of carotenoid limitation (first-hatched nestlings being less constrained than later-hatched nestlings). We discuss why nestlings would use supplemental carotenoids for increasing bare parts coloration rather than for responding to a PHA challenge, and the potential benefits for doing so in a parent-offspring communication context.This study was conducted under a licence delivered by the CRBPO (Museum National d’Histoire Naturelle). This work was financially supported by exchange programme no. 2009FR0021, between the CNRS (CEBC-CNRS UPR1934, Chizé, France) and the CSIC (IREC CSIC-UCLM-JCCM, Ciudad Real, Spain), and by the ‘Fondation Fyssen’ (grant to A.S.).Peer Reviewe

Phenotypic variation in nestlings of a bird of prey under contrasting breeding and diet conditions

Environmental conditions often vary in space and time, and this may explain variation in the expression of phenotypic traits related to individual quality, such as ornamental coloration. Furthermore, the direction and strength of the relationship between coloured trait expression and individual quality might vary under contrasting conditions. These issues have been explored in adult birds but much less so in nestlings, which are more likely to experience different selective pressures and different physiological trade-offs than adults. Here, we empirically investigated the effects of contrasting breeding and diet conditions on the expression of carotenoid-based colour traits displayed by marsh harrier (Circus aeruginosus) nestlings. We studied the variation in coloration, body condition, and immune responsiveness of nestlings in four populations over a 5-year period. We characterized spatiotemporal differences in rearing conditions experienced by C. aeruginosus nestlings in terms of breeding (laying date, clutch size, and number of nestlings hatched and fledged) and diet (percentage of mammal in diet and prey diversity) conditions. We found that breeding conditions influenced the co-variation between coloration and immune responsiveness in female nestlings, and that diet conditions influenced the condition-dependence of nestling coloration in later-hatched nestlings. In addition, breeding conditions influenced nestling body condition and immune responsiveness, whereas diet conditions influenced nestling coloration and body condition. Our study highlights that nestling phenotype (levels of signalling, circulating carotenoids, and immunity) varies both spatially and temporally, and that some of this variation is related to differences in breeding and diet conditions. Moreover, under contrasting conditions, the direction of the relationships between nestling carotenoid-based coloration and nestling quality may also vary. In order to fully understand the evolution and maintenance of colour traits in nestling birds, studies and experiments should ideally be replicated under contrasting rearing conditions.This study was conducted under a license delivered by the CRBPO (Muséum National d’Histoire Naturelle). A.S. was supported by a grant from the ‘Fondation Fyssen’ (Paris, France).Peer Reviewe

Carotenoid-based coloration, condition, and immune responsiveness in the nestlings of a sexually dimorphic bird of prey

In many birds, nestlings exhibit brightly colored traits that are pigmented by carotenoids. Carotenoids are diet limited and also serve important health-related physiological functions. The proximate mechanisms behind the expression of these carotenoid- pigmented traits are still poorly known, especially in nestlings with sexual size dimorphism. In these nestlings, intrabrood competition levels and growth strategies likely differ between sexes, and this may in turn influence carotenoid allocation rules. We used dietary carotenoid supplementation to test whether wild marsh harrier (Circus aeruginosus) nestlings were carotenoid limited and whether carotenoid allocation strategies varied between sexes, which differ in their size and growth strategies. When supplemented, nestlings used the supplemental carotenoids to increase their coloration independently of their sex. We showed that the condition dependence of the carotenoid level and the response to an immune challenge (phytohemagglutinin test) differed between sexes, possibly because sexual size dimorphism influences growth strategies and/ or intrabrood competition levels and access to different types of food. In this species, which often feeds on mammals, a tradeoff likely exists between food quantity (energy) and quality (carotenoid content). Finally, carotenoid-based coloration expressed in marsh harrier nestlings appeared to be indicative of immune responsiveness rather than condition, therefore potentially advertising to parents nestling quality or value rather than nutritional need.This study was conducted under a license granted by the Centre de Recherches sur la Biologie des Populations d’Oiseaux (Muséum National d’Histoire Naturelle). This work was financially supported by the Research Group 2155 (Centre National de la Recherche Scientifique [CNRS], Groupe de Recherche en Ecologie Comportementale) “Behavioral Ecology,” through a collaboration between the Centre d’E'tudes Biologiques de Chize (CNRS UPR1934, Chize, France) and the University of Bourgogne (CNRS UMR5561, Dijon). A.S. was supported by a grant from the Fondation Fyssen (Paris). L.P.-R. was supported by a Juan de la Cierva postdoctoral contract from the Spanish Ministerio de Ciencia e Innovación (JCI-2008-2059).Peer Reviewe

Carotenoids in nestling Montagu's harriers: variations according to age, sex, body condition and evidence for diet-related limitations

Carotenoids are colored pigments forming the basis of many avian social traits. Before their utilization carotenoids must be acquired through diet and mobilized for specific uses. The relationships between carotenoid-based coloration, circulating carotenoids and body condition have been well studied in adult birds, but little is known in nestlings. Here, we investigated variations in carotenoid-based coloration in a raptor nestling, the Montagu's harrier (Circus pygargus), both in captivity and in natural conditions, and within a vole (poor-carotenoid source and cyclic prey) specialist population. We studied these variations according to nestling age and sex, and possible limitations in carotenoid availability by comparing years of contrasted prey abundance and using carotenoid supplementation experiments. Captive nestlings, fed only with mice, were strongly carotenoid limited. Wild nestlings were also carotenoid limited, especially in a year of high vole abundance. Nestlings were in better condition but less colored during a peak vole abundance year than during a low vole abundance year, when harriers targeted more alternative preys (birds, insects). Thus, variation in vole abundance resulted in a de-coupling of body condition and carotenoid-based coloration in this population. This suggested that the positive relation between the body condition and carotenoid-based traits, typically found in adult birds, could be restricted to adults or nestlings of species that feed on carotenoid-rich food. Our results should stimulate more work on the functions and mechanisms of carotenoid-based traits in nestlings, which deserve more attention and most likely differ from those of adult birds. © Springer-Verlag 2009.This work was financially supported by the Research Group 2155 (CNRS, GDR) ‘Behavioural ecology’ through a collaboration between the Centre d’Etudes Biologique de Chizé (CNRS UPR1934, Chizé, France) and the University of Bourgogne (CNRS UMR5561, Dijon, France).Peer Reviewe

Adaptive significance of permanent female mimicry in a bird of prey

Permanent female mimicry, in which adult males express a female phenotype, is known only from two bird species. A likely benefit of female mimicry is reduced intrasexual competition, allowing female-like males to access breeding resources while avoiding costly fights with typical territorial males. We tested this hypothesis in a population of marsh harriers Circus aeruginosus in which approximately 40 per cent of sexually mature males exhibit a permanent, i.e. lifelong, female plumage phenotype. Using simulated territorial intrusions, we measured aggressive responses of breeding males towards conspecific decoys of females, female-like males and typical males. We show that aggressive responses varied with both the type of decoys and the type of defending male. Typical males were aggressive towards typical male decoys more than they were towards female-like male decoys; femalelike male decoys were attacked at a rate similar to that of female decoys. By contrast, femalelike males tolerated male decoys (both typical and female-like) and directed their aggression towards female decoys. Thus, agonistic responses were intrasexual in typical males but intersexual in female-like males, indicating that the latter not only look like females but also behave like them when defending breeding resources. When intrasexual aggression is high, permanent female mimicry is arguably adaptive and could be seen as a permanent 'non-aggression pact' with other males.This study was conducted under a licence delivered by the CRBPO (Museum National d'Histoire Naturelle, Paris, France). We thank the DREAL Poitou-Charentes and CNRS for funding this study, the Foundation Fyssen for a grant to A.S.Peer Reviewe