Frédéric Lacroix

Male health status, signalled by courtship display, reveals ejaculate quality and hatching success in a lekking species

1. The information content of secondary sexual traits and the benefits gathered by choosy females are at the heart of sexual selection theory. Indicator models of sexual selection assume that secondary sexual traits reflect the phenotypic/genetic quality of their bearers and that females gather benefits from choosing these high-quality males. 2. Here, we tested the idea that courtship display reflects the health status in a bird species with a lek-based mating system, the houbara bustard (Chlamydotis undulata undulata). A group of males was treated with the lipopolysaccharide (LPS) of the cell wall of the bacterium Escherichia coli during the seasonal peak of courtship display, while another group of males was injected with a phosphate-buffered saline solution (PBS) as a control. We then monitored the effect of the treatment on both courtship display and ejaculate quality. Finally, females were artificially inseminated with semen from LPS and PBS males, which allowed us to assess the effect of the immunological treatment on reproduction. 3. We found that the inflammatory challenge reduced courtship display and semen quality compared to controls. Interestingly, males that better resisted to the immune challenge in terms of courtship display also better resisted in terms of ejaculate quality. Early reproductive failure was increased when females were artificially inseminated with semen from immune-activated males. Failure of eggs laid by females inseminated with LPS semen was due to a reduced fertilization power of sperm of LPS males or to increased embryo mortality in the very early stage of embryo development. As a consequence, hatching rate was reduced for females inseminated with semen collected from LPS males. 4. These results show that by assessing male courtship display, females may gain insight into the current phenotypic/genetic quality of mates and gather fitness benefits in terms of reproductive success.

Habitat use and mating system of the houbara bustard (Chlamydotis undulata undulata) in a semi-desertic area of North Africa: implications for conservation

Studies of the movements and home-ranges of houbara bustards (Chlamydotis undulata undulata) showed sexual and seasonal differences in the use of space, with a polygynous mating system similar to an ‘exploded-lek’ or a ‘resource-defence-polygyny’, that remains undefined. We used the arthropod biomass as an index of the trophic quality of six defined habitats and we radio-tracked 7 females and 13 males to test whether sexual and seasonal variations in habitat use were related to resource availability, and to verify if critical resources for breeding females were monopolised by males. We analysed habitat selection in both sexes separately. We used the habitat type composition of buffer zones around radio-locations to study annual and seasonal habitat selection and to identify preferred habitats, using the chi-square goodness-of-fit test. Habitat use between sexes and between seasons were compared using MANOVA based on log-ratios of habitat proportions. During the year, and in each season, both sexes appeared to be significantly selective for habitats in comparison to their availability. But males avoided esparto grass, while females used all habitats. Habitat use differed between sexes in the breeding season, but not in the non-breeding season. In spring, when food resources were abundant and uniformly distributed in space, males preferred ‘temporarily flooded areas’ and females preferred ‘reg with tall perennials’ that offered both food and cover for brooding. Critical resources were not monopolised by males and the mating system fulfilled the definition of the ‘exploded-lek’. Leks are key sites for reproduction and should be considered as priority areas in further conservation plans.

Landscape and human influences on the distribution of the endangered North African houbara bustard ( Chlamydotis undulata undulata ) in Eastern Morocco

The distribution and global habitat association of the North African houbara bustard (Chlamydotis undulata sensu stricto) were studied for the first time in a large semi-arid steppe-land region in eastern Morocco. The study area has been protected from hunting for 6 years, but was still under significant pressure from grazing activities. Houbara distribution was assessed using point count surveys conducted during the 2002 breeding season and compared to natural- and human-related predictors. The hierarchy and quantification of influences was evaluated using a discriminant function analysis. Micro-topography first drove houbara bustard distribution, since birds were usually found in open flat tracts allowing visibility over a long distance for the prevention of potential predator approaches, but also for breeding males to be seen by conspecifics. ‘Flooding surfaces’ presenting concealment possibilities, as well as readily available food resources, were secondly sought. Proximity to wells was a surrogate to human presence and pastoral activity influences and appeared to affect houbara bustard distribution. The weight of human disturbance on houbara distribution is highlighted and it is recommended that this should be considered in conservation plans.

Meteorological conditions influence short‐term survival and dispersal in a reinforced bird population

A high immediate mortality rate of released animals is an important cause of translocation failure (‘release cost’). Post-release dispersal (i.e. the movements from the release site to the first breeding site) has recently been identified as another source of local translocation failure. In spite of their potential effects on conservation program outcomes, little is known about the quantitative effects of these two sources of translocation failure and their interactions with environmental factors and management designs.[br/] Based on long-term monitoring data of captive-bred North African houbara bustards Chlamydotis undulata undulata (hereafter, houbara) over large spatial scales, we investigated the relative effects of release (e.g. release group size, period of release), individual (e.g. sex and body condition) and meteorological (e.g. temperature and rainfall) conditions on post-release survival (n = 957 individuals) and dispersal (n = 436 individuals).[br/] We found that (i) rainfall and ambient air temperature had, respectively, a negative and a positive effect on houbara post-release dispersal distance; (ii) in interaction with the release period, harsh meteorological conditions had negative impact on the survival of houbara; (iii) density-dependent processes influenced the pattern of departure from the release site; and (iv) post-release dispersal distance was male-biased, as natal dispersal of wild birds (although the dispersal patterns and movements may be influenced by different processes in captive-bred and in wild birds).[br/] Synthesis and applications. Our results demonstrate that post-release dispersal and mortality costs in translocated species may be mediated by meteorological factors, which in turn can be buffered by the release method. As the consequences of translocation programs on population dynamics depend primarily upon release costs and colonization process, we suggest that their potential interactions with meteorological conditions must be carefully addressed in future programs (i) through monitoring of short-term post-release mortality to understand its link with environmental conditions, (ii) by carefully choosing the season of release to minimize exposition of inexperienced individuals to harsh conditions and (iii) by generalizing the use of long-term weather forecast to adapt release effort and staggering releases over several years to buffer meteorological effects.

Does recognized genetic management in supportive breeding prevent genetic changes in life‐history traits?

Supportive breeding is one of the last resort conservation strategies to avoid species extinction. Management of captive populations is challenging because several harmful genetic processes need to be avoided. Several recommendations have been proposed to limit these deleterious effects, but empirical assessments of these strategies remain scarce. We investigated the outcome of a genetic management in a supportive breeding for the Houbara Bustard. At the phenotypic level, we found an increase over generations in the mean values of gamete production, body mass and courtship display rate. Using an animal model, we found that phenotypic changes reflected genetic changes as evidenced by an increase in breeding values for all traits. These changes resulted from selection acting on gamete production and to a lesser extent on courtship display. Selection decreased over years for female gametes, emphasizing the effort of managers to increase the contribution of poor breeders to offspring recruited in the captive breeding. Our results shed light on very fast genetic changes in an exemplary captive programme that follows worldwide used recommendations and emphasizes the need of more empirical evidence of the effects of genetic guidelines on the prevention of genetic changes in supportive breeding.

Assessing habitat and resource availability for an endangered desert bird species in eastern Morocco: the Houbara Bustard

In Morocco we tested the consistency between an a priori habitat classification based on topography, hydrology, vegetation structure and composition, and an a posteriori classification based on arthropod assemblages, in a plain supporting wild endangered Houbara Bustards. According to vegetation structure, we defined seven a priori habitats that differed significantly in perennial cover and height. A multivariate multiple regression analysis showed a significant relationship between arthropod assemblages and vegetation structure. Canonical Analyses of Principal Coordinates, conducted simultaneously on direct searches of arthropods and trapping data, showed significant differences between assemblages in both cases, and produced two similar constrained ordinations of six a posteriori habitats: esparto grass (Stipa tenacissima), temporarily flooded areas, fields, “reg” with short perennials, “reg” with tall perennials and wadis. The two sampling methods reflected a dominance of ants and beetles. Arthropod biomasses increased significantly in spring and then decreased significantly in summer for beetles, and in autumn for ants. No strong differences appeared between habitats within seasons, especially in spring, indicating a uniform distribution of food resources during the Houbara breeding season. The “reg” with short perennials had the highest ant biomass in summer. This “reg” and fields also supported the highest arthropod biomass in autumn. Variation in arthropod biomass was a pertinent factor that should be integrated into Houbara habitat selection studies. The definition of habitat availability based on easily identifiable landscape units, combined with empirical tests on arthropod communities provided an accurate classification for habitat selection studies and conservation planning.

Conservation genetics of Houbara Bustard (Chlamydotis undulata undulata): population structure and its implications for the reinforcement of wild populations

The major decline of Houbara Bustards—sensu lato—throughout their range has led to their classification as ‘vulnerable’ on the IUCN Red List. Within this context, a captive breeding program was established in Morocco to restock North African wild populations of Houbara Bustard (Chlamydotis undulata undulata). At present, founders originate from locations that are currently being reinforced through the addition of captive bred individuals. However, it is planned to restock others areas of the species’ range. Before this could be considered, an accurate knowledge of the genetic structure of the wild recipient population is essential to delineate potential conservation units. We therefore sampled populations throughout most of the remaining range, and used several methods to evaluate their genetic differentiation by means of both mtDNA and microsatellite markers. Very little genetic differentiation was found for both genetic markers (Φst ranged from −0.181 to 0.118 and Fst ranged from −0.004 to 0.019). This suggests that C. u.undulata populations could be managed as a single Conservation Unit.

Quantitative genetics of sexual display, ejaculate quality and size in a lekking species

The investment into extravagant sexual display and competitive sperm are two essential components of pre- and post-copulatory sexual selection. Even though the selective forces acting on sexual display and sperm characteristics have been extensively studied in recent years, the genetic architecture underlying the expression of these traits has been rarely explored. Here, we estimated the genetic variances and covariances of traits linked with ejaculate size and quality, and sexual display in the houbara bustard (Chlamydotis undulata undulata, Jacquin 1784). Using a very large pedigree-based data set, we show that sexual signalling and ejaculate size (but not ejaculate quality) are heritable and genetically positively correlated. The matrix of genetic covariances also provided support for some across-sex correlations: male and female gamete numbers are positively correlated, and more surprisingly, male display and female gamete numbers are also positively correlated. These results can have important implications for the understanding of the evolution of sperm traits and sexual display in animals.

Immune-Mediated Change in the Expression of a Sexual Trait Predicts Offspring Survival in the Wild

Background The “good genes” theory of sexual selection postulates that females choose mates that will improve their offsprings fitness through the inheritance of paternal genes. In spite of the attention that this hypothesis has given rise to, the empirical evidence remains sparse, mostly because of the difficulties of controlling for the many environmental factors that may covary with both the paternal phenotype and offspring fitness. Here, we tested the hypothesis that offspring sired by males of a preferred phenotype should have better survival in an endangered bird, the houbara bustard (Chlamydotis undulata undulata). Methodology/Principal Findings We tested if natural and experimentally-induced variation in courtship display (following an inflammatory challenge) predicts the survival of offspring. Chicks were produced by artificial insemination of females, ensuring that any effect on survival could only arise from the transfer of paternal genes. One hundred and twenty offspring were equipped with radio transmitters, and their survival monitored in the wild for a year. This allowed assessment of the potential benefits of paternal genes in a natural setting, where birds experience the whole range of environmental hazards. Although natural variation in sire courtship display did not predict offspring survival, sires that withstood the inflammatory insult and maintained their courtship activity sired offspring with the best survival upon release. Conclusions This finding is relevant both to enlighten the debate on “good genes” sexual selection and the management of supportive breeding programs.

Quantitative Genetics of the Aging of Reproductive Traits in the Houbara Bustard

Do all traits within an organism age for the same reason? Evolutionary theories of aging share a common assumption: the strength of natural selection declines with age. A corollary is that additive genetic variance should increase with age. However, not all senescent traits display such increases suggesting that other mechanisms may be at play. Using longitudinal data collected from more than 5400 houbara bustards (Chlamydotis undulata) with an exhaustive recorded pedigree, we investigated the genetics of aging in one female reproductive trait (egg production) and three male reproductive traits (courtship display rate, ejaculate size and sperm viability), that display senescence at the phenotypic level. Animal models revealed an increase in additive genetic variance with age for courtship display rate and egg production but an unexpected absence of increased additive genetic variance for ejaculate size and no additive genetic variance for sperm viability. Our results suggest that the mechanisms behind the senescence of some traits are linked with a change in genetic expression, whereas for some other traits, aging may result from the constraints associated with physiological wear and tear on the organism throughout the life of the individual.