Proximate and ultimate drivers of breeding-group choice and reproductive success in male spotted hyenas (Crocuta crocuta)

In group-living species, the choice of the breeding group and the social rank in the hierarchy of the group strongly influence an individual’s fitness. Yet the causes and consequences of variation in breeding-group choice and dispersal propensity, and the proximate mechanisms through which social rank influences an individual’s ability to access mates and reproduce remain poorly understood. This thesis has three main aims: (i) identify the drivers of the coexistence of dispersal and philopatry among males in the spotted hyena (Crocuta crocuta), a large, group-living carnivore; (ii) assess whether and how social rank and social and physiological constraints influence reproductive investment and success in male hyenas; (iii) improve the applicability of non-invasive hormone concentration measurements. The thesis combines long-term data on the behaviour, physiology, survival and reproductive success of male spotted hyenas with demographic data from all eight social groups of a free-ranging hyena population in Tanzania. In Chapter 3, I show that philopatric male and dispersers are of similar phenotypic quality, follow the same process and apply the same rules to choose and settle in a breeding group, and have similar survival and reproductive success. I also show that social rank is a strong determinant of male access to mates and reproductive success in spotted hyenas. Philopatric males gain reproductive benefits associated with their high social rank and these benefits increase the propensity of males to choose their natal group as a breeding group. The results demonstrate that the distribution of breeding females across natal and nonnatal groups is an important determinant of dispersal patterns and of the coexistence of philopatry and dispersal in male spotted hyenas. In Chapter 4, I develop a novel method to standardise hormone metabolite concentration measurements when substantial changes in the accuracy of an immunoassay occur. The method is based on repeated assaying of a small number of samples and restores the comparability of the measurements. The method constitutes an effective alternative to the often impracticable re-assaying of complete sample sets. In Chapter 5, I show that males with a high social rank are less constrained by physiological stress than low-ranking males, owing to their greater opportunities to express dominance and enjoy the buffering effect of social bonds. This allows high-ranking males, including philopatric males, to allocate more time than low-ranking males to fitness-enhancing social and sexual activities, and to focus their sexual investment on females of high reproductive value. These results are consistent with the results of Chapter 3 and may explain why philopatric males and high-ranking immigrants are particularly successful at siring offspring with females of high reproductive value. The thesis provides insights into (i) the role of demographic variability and the distribution of breeding partners in driving the evolution of dispersal and in shaping dispersal patterns within populations; (ii) the traits that underpin differences in competitive ability and reproductive performance between males of different social rank; and (iii) the role of social rank and of social and physiological constraints in shaping differences in life history and reproductive success among males in group-living species.Bei gruppenlebenden Arten wird die Fitness von Individuen stark durch die Wahl der Fortpflanzungsgruppe und den sozialen Rang in der Hierarchie der Gruppe beeinflusst. Die Ursachen und Folgen von Unterschieden in der Wahl der Fortpflanzungsgruppe und der Abwanderungsneigung sowie die Mechanismen, durch die der soziale Rang den Zugang zu Paarungspartnern und den Fortpflanzungserfolg beeinflusst, sind weitgehend unbekannt. Diese Arbeit hat drei Hauptziele: (i) Ursachen für die Koexistenz von Abwanderung und Ortstreue (Philopatrie) bei Männchen der Tüpfelhyäne (Crocuta crocuta), einem großen, gruppenlebenden Raubtier, zu identifizieren; (ii) den Einfluss des sozialen Ranges und sozialer und physiologischer Eigenschaften auf die Investitionen in die Fortpflanzung und den Fortpflanzungserfolg bei Tüpfelhyänen-Männchen zu ermessen; (iii) die Anwendbarkeit von nicht-invasiven Hormonkonzentrationsmessungen zu verbessern. Die Arbeit verbindet Langzeitdaten über das Verhalten, die Physiologie, das Überleben und den Fortpflanzungserfolg von Tüpfelhyänen-Männchen mit demographischen Daten aus allen acht Clans einer freilebenden Hyänenpopulation in Tansania. In Kapitel 3 zeige ich, dass abgewanderte und philopatrische Tüpfelhyänen-Männchen von ähnlicher phänotypischer Qualität sind, die gleichen Prozesse und Regeln anwenden, um eine Fortpflanzungsgruppe auszuwählen und sich darin niederzulassen, und ähnliche Überlebenswahrscheinlichkeiten und Fortpflanzungserfolge haben. Ich zeige auch, dass der soziale Rang den Zugang zu Paarungspartnern und den Fortpflanzungserfolg beeinflusst, dass philopatrische Männchen durch ihren hohen sozialen Rang einen hohen Fortpflanzungserfolg haben, und dass die Vorteile von Ortstreue die Wahrscheinlichkeit der Männchen erhöht, ihre Geburtsgruppe als Fortpflanzungsgruppe auszuwählen. Die Ergebnisse zeigen, dass die Anzahl der Paarungspartner in der Geburts- und anderen Gruppen das Abwanderungsverhalten und die Abwanderungshäufigkeit bestimmt und die Koexistenz von Abwanderung und Ortstreue bei Tüpfelhyänen-Männchen begründet. In Kapitel 4 entwickle ich eine neuartige Methode zur Standardisierung der Messung von Hormonmetabolitenkonzentrationen wenn wesentliche Änderungen in der Messgenauigkeit eines Immunoassays auftreten. Das Verfahren basiert auf der bei jeder Messung wiederholten Analyse einer kleinen Anzahl von Proben und stellt die Vergleichbarkeit der Messungen her. Es ist eine effektive und effiziente Alternative zur oft undurchführbaren wiederholten Analyse aller Proben. In Kapitel 5 zeige ich, dass Männchen mit einem hohen sozialen Rang mehr Möglichkeiten haben, Dominanz auszuüben und von der Pufferwirkung sozialer Bindungen zu profitieren als Männchen mit einem niedrigeren Rang. Hochrangige Männchen werden dadurch weniger stark durch physiologischen Stress eingeschränkt als tieferrangige Männchen. Dies ermöglicht es hochrangigen Männchen, einschließlich philopatrischen Männchen, mehr Zeit in fitnessfördernde soziale und sexuelle Aktivitäten zu investieren als tiefer rangige Männchen und besonders viel in Weibchen mit hohem Fortpflanzungswert zu investieren. Diese Ergebnisse stehen im Einklang mit den Ergebnissen von Kapitel 3 und können erklären, warum philopatrische Männchen und hochrangige Einwanderer besonders häufig Nachkommen mit Weibchen von hohem Fortpflanzungswert zeugen. Die Arbeit liefert Einblicke in (i) die Rolle der demographischen Variabilität und der Verteilung von Paarungspartnern für die Evolution von Abwanderung und Philopatrie und die Entstehung von Abwanderungsmustern auf Populationsebene, (ii) Merkmale, die Unterschiede in der Konkurrenzfähigkeit und der Investition in Fortpflanzung zwischen Männchen unterschiedlichen sozialen Ranges verursachen, und (iii) die Rolle des sozialen Ranges und sozialer und physiologischer Eigenschaften bei der Entstehung von Unterschieden in der Lebensgeschichte und des Fortpflanzungserfolgs zwischen Männchen bei gruppenlebenden Arten

Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals

Funding: Hoge Veluwe great tits: the NIOO-KNAW, ERC, and numerous funding agencies; Wytham great tits: Biotechnology and Biological Sciences Research Council, ERC, and the UK Natural Environment Research Council (NERC).The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.PostprintPeer reviewe

Sex and dominance: How to assess and interpret intersexual dominance relationships in mammalian societies

The causes and consequences of being in a particular dominance position have been illuminated in various animal species, and new methods to assess dominance relationships and to describe the structure of dominance hierarchies have been developed in recent years. Most research has focused on same-sex relationships, however, so that intersexual dominance relationships and hierarchies including both sexes have remained much less studied. In particular, different methods continue to be employed to rank males and females along a dominance hierarchy, and sex biases in dominance are still widely regarded as simple byproducts of sexual size dimorphism. However, males and females regularly compete over similar resources when living in the same group, and sexual conflict takes a variety of forms across societies. These processes affect the fitness of both sexes, and are mitigated by intersexual hierarchies. In this study, we draw on data from free-ranging populations of nine species of mammals that vary in the degree to which members of one sex dominate members of the other sex to explore the consequences of using different criteria and procedures for describing intra- and intersexual dominance relationships in these societies. Our analyses confirmed a continuum in patterns of intersexual dominance, from strictly male-dominated species to strictly female-dominated species. All indices of the degree of female dominance were well correlated with each other. The rank order among same-sex individuals was highly correlated between the intra- and intersexual hierarchies, and such correlation was not affected by the degree of female dominance. The relative prevalence of aggression and submission was sensitive to variation in the degree of female dominance across species, with more submissive signals and fewer aggressive acts being used in societies where female dominance prevails. Thus, this study provides important insights and key methodological tools to study intersexual dominance relationships in mammals

Kinship and similarity drive coordination of breeding-group choice in male spotted hyenas

When and where animals reproduce influences the social, demographic and genetic properties of the groups and populations they live in. We examined the extent to which male spotted hyenas (Crocuta crocuta) coordinate their breeding-group choice. We tested whether their propensity to settle in the same group is shaped by passive processes driven by similarities in their socio-ecological background and genotype or by an adaptive process driven by kin selection. We compared the choices of 148 pairs of same-cohort males that varied in similarity and kinship. We found strong support for both processes. Coordination was highest (70% of pairs) for littermates, who share most cumulative similarity, lower (36%) among peers born in the same group to different mothers, and lowest (7%) among strangers originating from different groups and mothers. Consistent with the kin selection hypothesis, the propensity to choose the same group was density dependent for full siblings and close kin, but not distant kin. Coordination increased as the number of breeding females and male competitors in social groups increased, i.e. when costs of kin competition over mates decreased and benefits of kin cooperation increased. Our results contrast with the traditional view that breeding-group choice and dispersal are predominantly solitary processes

Does chromosomal change restrict gene flow between house mouse populations (Mus musculus domesticus)? Evidence from microsatellite polymorphisms

International audienceChromosomal change is recognized as an important force in speciation-with-gene-flow models. Although Robertsonian (Rb) translocations contribute to hybrid unfitness and modify recombination patterns, they are generally not considered as efficient as inversions in reducing gene flow. The present study analyses two hybridizing chromosomal races of the house mouse (Mus musculus domesticus), one carrying nine Rb fusions (2n = 22) and the other carrying the ancestral karyotype (2n = 40). Chromosomal heterozygosity involves simple meiotic configurations, the underdominance of which is not as efficient in promoting speciation as more complex chromosomal differences. The pattern of divergence between these races was investigated using 32 microsatellite loci distributed over all autosomes. The results highlighted a relatively large differentiation between the two chromosomal races. The contribution of variation in recombination patterns to this differentiation was supported by the contrasting levels of divergence between proximal vs. non-proximal microsatellite loci. Clinal analyses of the Rb fusions through the hybrid zone uncovered differences in steepness between metacentrics, suggesting associated differences in selection which did not involve linked genic incompatibilities. This study illustrates the significant role of Rb-associated changes in recombination in promoting or maintaining divergence between chromosomal races of the house mouse

The eco-evolutionary landscape of power relationships between males and females

International audienceIn animal societies, control over resources and reproduction is often biased towards one sex. Yet, the ecological and evolutionary underpinnings of male–female power asymmetries remain poorly understood. We outline a comprehensive framework to quantify and predict the dynamics of male–female power relationships within and across mammalian species. We show that male–female power relationships are more nuanced and flexible than previously acknowledged. We then propose that enhanced reproductive control over when and with whom to mate predicts social empowerment across ecological and evolutionary contexts. The framework explains distinct pathways to sex-biased power: coercion and male-biased dimorphism constitute a co-evolutionary highway to male power, whereas female power emerges through multiple physiological, morphological, behavioural, and socioecological pathways

Why do some males choose to breed at home when most other males disperse?

Dispersal is a key driver of ecological and evolutionary processes. Despite substantial efforts to explain the evolution of dispersal, we still do not fully understand why individuals of the same sex of a species vary in their propensity to disperse. The dominant hypothesis emphasizes movements and assumes that leaving home (dispersal) and staying at home (philopatry) are two alternative strategies providing different fitness. It suggests that only individuals of high phenotypic quality can pursue the most beneficial strategy; the others are left to do a “best-of-a-bad” job. An alternative hypothesis emphasizes settlement decisions and suggests that all individuals pursue a single strategy of choosing the breeding habitat or group with the highest fitness prospects; choosing the natal group (philopatry) and choosing a nonnatal group (dispersal) are then outcomes of these decisions. We tested both hypotheses using a long-term study of a free-ranging population of a group-living carnivore, the spotted hyena. We combined demographic data with data on dispersal-relevant phenotypic traits, breeding-group choice, survival, and reproductive success of 254 males. Our results contradict the best-of-a-bad-job hypothesis: philopatric males and dispersers were of similar phenotypic quality, had similar fitness, and applied similar settlement rules based on the fitness prospects in groups. Our findings demonstrate that the distribution of breeding partners can be more important in shaping dispersal patterns than the costs associated with the dispersal movement. The study provides novel insights into the processes leading to the coexistence of philopatry and dispersal within the same sex of a species

Social support drives female dominance in the spotted hyaena

International audienceIdentifying how dominance within and between the sexes is established is pivotal to understanding sexual selection and sexual conflict. In many species, members of one sex dominate those of the other in one-on-one interactions. Whether this results from a disparity in intrinsic attributes, such as strength and aggressiveness, or in extrinsic factors, such as social support, is currently unknown. We assessed the effects of both mechanisms on dominance in the spotted hyaena (Crocuta crocuta), a species where sexual size dimorphism is low and females often dominate males. We found that individuals with greater potential social support dominated one-on-one interactions in all social contexts, irrespective of their body mass and sex. Female dominance emerged from a disparity in social support in favour of females. This disparity was a direct consequence of male-biased dispersal and the disruptive effect of dispersal on social bonds. Accordingly, the degree of female dominance varied with the demographic and kin structure of the social groups, ranging from male and female co-dominance to complete female dominance. Our study shows that social support can drive sex-biased dominance and provides empirical evidence that a sex-role-defining trait can emerge without the direct effect of sex

The interplay between social rank, physiological constraints and investment in courtship in male spotted hyenas

In many animal societies, dominant males have a higher reproductive success than subordinate males. The proximate mechanisms by which social rank influences reproductive success are poorly understood. One prominent hypothesis posits that rank-related male attributes of attractiveness and fighting ability are the main mediators of reproductive skew. Yet, empirical evidence in support of this hypothesis is limited. An alternative hypothesis emphasises the inherent social dimension of dominance relationships and posits that the relationship between male social rank and reproductive success is mediated by the physiological costs of male?male competition. This has not been tested in systems in which the two hypotheses can be disentangled. We investigated the interplay between male social rank, physiological costs and male investment in social and sexual activities. We used measurements of faecal glucocorticoid metabolite concentrations (fGMC) as biomarkers of physiological costs and long-term behavioural data of 319 males in free-ranging spotted hyenas Crocuta crocuta, a species in which male access to females and reproductive success do not depend on physical attributes. When males courted females and interacted with male competitors, low-ranking males had higher fGMC than high-ranking males. In contrast, fGMC did not vary with social rank when males were alone or when they courted females and competitors were absent. Low-ranking males minimised their exposure to physiologically costly intrasexual competition; they spent more time alone and less time engaging in social and sexual activities than did high-ranking males. They also invested less than high-ranking males in courting the most contested and highest-quality females. Our findings demonstrate that the physiological costs of intrasexual competition in male spotted hyenas vary with social rank and shape behavioural trade-offs between the allocation of time and physiological resources to social integration, reproduction and self-maintenance. Our study suggests that physiological and social constraints play a pivotal role in the emergence of rank-related male reproductive success. The study provides insights into how the social organisation and breeding system shape physiological constraints and patterns of reproductive skew within and between species. A free Plain Language Summary can be found within the Supporting Information of this article