Life history and social behaviour

The life history of an individual sets the stage for key adaptations to survive and successfully reproduce. Each stage is characterised by the environment, such as the maternal environment, and shaped by intra-specific evolutionary conflicts within and between generations. Intra-specific evolutionary conflicts include disputes over allocation of parental investment to different broods and offspring (parent-offspring conflict) and competition between offspring (sibling rivalry). In social species, the maternal environment and intra-specific conflicts are often a more powerful force of selection than abiotic or other biotic sources. Thus, an understanding of the evolutionary effects of the maternal environment and intra-specific conflicts on behaviour, communication, and reproductive success of individuals contributes to an understanding of the adaptive value of mammalian life histories. A final point is to understand the processes which limit life histories, such as senescence, and their underlying mechanisms.

The social environment as a fitness-determining factor: Group living

Group-living seems to be of advantage in almost all species of mammals. Indeed, individuals of some species collaborate excessively; for example spotted hyenas during foraging or suckling bats when forming clusters in daytime roosts. Group hunting has as well been suggested for bats, yet nocturnal animals are constrained in the use of visual cues to coordinate a group hunt. Using playback experiments, we demonstrated that hunting lesser bulldog bats, Noctilio albiventris, eavesdrop on the echolocation calls of successfully foraging conspecifics. This is particularly advantageous for this bat species because N. albiventris hunts for swarming insects over large water bodies, a highly ephemeral food source. Thus, listening to the calls of successful conspecifics may shorten the search phase of foraging bats.
One of the most extreme forms of cooperation in mammals can be found in the eusocial naked mole rat (Heterocephalus glaber). Comparable to bees and ants, in naked mole rat colonies with up to 300 members only one individual – the queen – gives birth to the entire offspring of the group. The colony cooperates in digging subterranean tunnel systems, foraging and rearing the offspring of the queen.

Maternal effects

Life history theory predicts that mothers should provide their offspring with a privileged upbringing if this enhances their offspring’s and their own fitness. In many group-living mammals, high-ranking mothers provide their offspring with a privileged upbringing. Using long-term demography and paternity data on a population of spotted hyenas Crocuta crocuta, we showed that dispersing sons gain fitness benefits during adulthood from such privileges, that is, they benefited from a ‘silver spoon’ effect. In this complex, female-dominated society, high-born sons grew at higher rates, were more likely to disperse to clans offering the best fitness prospects, started reproducing earlier, and had a higher reproductive value than lower-born sons.

Inheritance of social status

Social status is a key phenotypic trait determining access to resources and fitness-relevant parameters. In many mammalian societies, offspring acquire a status at adulthood similar to that held by their mother (‘rank inheritance’) and obtain the fitness benefits associated with it. Using cases of offspring adoption in the spotted hyena, we demonstrated that the rank of adopted offspring was very similar to that of their surrogate mother and quite different from the rank of their genetic mother. The mechanism responsible for rank inheritance is postnatal maternal behavioural support rather than direct genetic effects or pre-natal hormonal effects in the womb: the young ‘learn’ during adolescence which group members they can dominate when their mother helps them win contests against members that are subordinate to the mother.

Social behaviour and reproductive tactics

Fetal sex predetermination acts against the random, equal opportunity both conceptus sexes have by nature. Under a wide variety of circumstances, populations shift their birth sex ratio from the expected unity. If the (as yet unknown) mechanisms through which this is done could be elucidated and thus manipulated, they would become an invaluable conservation tool. For instance, some of the captive Asian and African elephant populations in Europe and North America produce more male offspring, particularly when pregnancies were initiated through artificial insemination, leading to 83% male offspring. It was previously thought that such shifts in sex ratio were solely under the influence of females. We examined whether males may also contribute to skewing offspring sex ratio by analysing the ratio of X- and Y-chromosome bearing spermatozoa in ejaculates of captive pygmy hippopotamus (Choeropsis liberiensis) populations in which 42.5% of offspring are males. Only about 43% of the spermatozoa carried Y-chromosome, a significant underrepresentation. To our surprise there appears to occur little or no antagonistic sexual conflict between the sexes, indicating that males possess a mechanism to adjust the ratio of X- and Y-chromosome bearing spermatozoa in the ejaculate.

Dispersal

Dispersal of offspring from the home group or home area is a key life history decision. In most species, dispersal is strongly biased towards one sex; in group-living mammals, dispersal is normally male-biased. In theory this bias could be a response by males to female mate preferences, competition for access to females or resources, or the result of males avoiding inbreeding. In spotted hyenas, we simultaneously assessed all these factors and measured the long-term fitness consequences of male dispersal decisions. We demonstrated that male-biased dispersal resulted from an adaptive response by males to simple female mate-choice rules. By applying these rules, females effectively avoid inbreeding without the need to discriminate directly against close kin or favour immigrant males. The greater sac-winged bat, Saccopteryx bilineata, is one of the few examples of a mammal with female-biased dispersal. Colonies of S. bilineata show a patrilineal colony structure, and female dispersal helps to avoid father-daughter inbreeding, as male tenure exceeds female age at first breeding in this species. Further, long-term paternity studies in several colonies revealed that male group size renders direct fitness benefits for males that outweigh the cost of competing with related males for access to territories and mates. Hyenas and bats provide striking examples of how life-history constraints and group living lead to opposite patterns in dispersal behaviour.

Sibling rivalry

In most birds and many mammals, offspring of a brood compete for access to food. Spotted hyenas are one of the best mammalian models to study this issue. During periods of low prey abundance, mothers often fail to provide sufficient milk to nourish both cubs of a twin litter. Theoretically, dominant cubs would then benefit from consuming also some, or all, of the subordinate’s share, even if this leads to the death of the subordinate (siblicide). Using data from 19 cub cohorts and growth rates of 195 twin litter cubs, we showed that the incidence of siblicide increased as average cohort growth rate declined. When both cubs were alive, maternal input in litters where siblicide occurred was lower than and the mean share of dominant sibs was higher than that of dominant sibs in non-siblicide litters. After siblicide, growth rates and expected survival of siblicide victors increased. These results suggest that high maternal input in lactation has favoured the evolution of facultative siblicide. When looking in detail at the dynamics of the interactions between dominant and subordinate sibs, we discovered that the best explanation for the establishment and maintenance of dominance between littermates are trained loser effects rather than intrinsic asymmetries already present at birth (such as birth order, birth mass or sex of offspring). We also demonstrated that the behaviour of subordinates drives the dynamics of the relationship between littermates: when the prospect of starvation increases, subordinates become more assertive and are less likely to submit to dominance conventions, dominants exert only incomplete control over subordinates, female subordinates are better competitors than male subordinates and in times of hunger subordinates of dominant sisters are more assertive than subordinates of dominant males.

Mechanisms and functional consequences of aging / senescence

Ageing in organisms is defined as a decrease in physiological function with age which results from cellular senescence due to an accumulation of biochemical changes in molecules required for normal cellular function. The rate at which this damage accumulates is modulated by ‘anti-ageing’ biochemical mechanisms that either prevent damage or repair damage once it has occurred. These mechanisms utilise body resources that otherwise could be used for other important life functions such as growth, reproduction or immunocompetence, thus life-history trade-offs are expected in relation to investment of body resources in ‘anti-aging’ mechanisms and other functions.

From an evolutionary perspective, ageing is difficult to explain because in general, traits that decrease lifespan should be selected against. Factors that determine or modulate rates of cellular senescence and the aging of organisms have been studied mostly in humans and short-lived model laboratory organisms such as the fruit fly Drosophila melanogaster, the nematode Caenorhabditis elegans and rodents. Even though natural selection will clearly act on these factors, there have been relatively few studies that have investigated aging in wildlife populations subject to natural selection.

Our research on aging is focused on mammalian wildlife species likely to provide novel insights on aging processes and how these are impacted by life history trade-offs. They include the naked mole rat Heterocephalus glaber and various bat species that have significantly longer life-spans than expected in relation to their body size, and the spotted hyena Crocuta crocuta, that invests an exceptionally high level of maternal body resources in rearing offspring in terms of lactation in comparison to other carnivore species.

Naked mole rats represent an extreme outlier to this rule. They are rodents approximately the size of a mouse, yet they may live for up to 30 years. Even more surprisingly, they contradict the theory according to which an organism invests its resources either into producing numerous offspring or into an extended life span. A naked mole rat queen - together with one or two males, the pashas - produces the entire offspring of a colony; up to 1100 birth of one single queen have been recorded in captivity. Furthermore, the queen alone lactates, and constantly has to defend her position within the colony. Despite these high energetic demands, her life expectancy (and also that of the pashas) exceeds that of the colony members. To gain insight into the underlying biochemical mechanism of this prolonged lifespan, a team of researchers at the IZW converts male and female naked mole rat workers into new queens and pashas: housed in pairs, separated from their native colony and its queen and pashas, they may found a new colony. By exploring the associated changes in transcriptome during this transition, we aim to decipher the anti-ageing strategies of naked mole rats. The results, apart from uncovering amazing evolutionary adaptations, may prove to be relevant for human ageing research as well.

Senescence is the increase in the probability of death and the decline in fitness caused by an accumulation of physiological degradation with increasing age. Previously, senescence was considered to be phenomenon restricted to humans, yet this notion has been recently replaced by the recognition that senescence is widespread among wildlife species and birds. Selection should act strongly against any senescence, since senescence impairs rather than improves an individual’s fitness. Some mammalian taxa, such as bats, live longer than predicted based on their body size. These outliers may unravel some important underlying mechanisms that promote longevity. For example, bats are long-lived even though they exhibit high mass-specific metabolic rates. Thus, the longevity of bats argues against the relevance of toxic by-products and an increase of oxidative damage caused by high metabolic rates. Until now, it is unclear why bats, in particular, are long-lived.

Selected publications

Benhaiem S, Hofer H, Kramer-Schadt S, Brunner E, East ML (2012) Sibling rivalry: training effects, emergence of dominance and incomplete control. Proc R Soc Lond B 279: 3727-3735.

Nagy M, Knörnschild M, Voigt CC, Mayer F (2012) Male greater sac-winged bats gain direct fitness benefits when roosting in multimale colonies. Behav Ecol 23: 597-606.

Saragusty J, Hermes R, Hofer H, Bouts T, Göritz F, Hildebrandt TB (2012) Male pygmy hippopotamus influence offspring sex ratio. Nat Commun 3: 697.

Höner OP, Wachter B, Hofer H, Wilhelm K, Thierer D, Trillmich F, Burke T, East ML (2010) The fitness of dispersing spotted hyaena sons is influenced by maternal social status. Nat Commun 1: 60.

Dechmann DKN, Heucke SL, Guggioli L, Safi K, Voigt, CC, Wikelski M (2009) Experimental evidence for group hunting via eavesdropping in echolocating bats. Proc R Soc Lond B 276: 2721-2728.

East ML, Höner OP, Wachter B, Wilhelm K, Burke T, Hofer H (2009) Maternal effects on offspring social status in spotted hyenas. Behav Ecol 20: 478-483.

Höner OP, Wachter B, East ML, Streich WJ, Wilhelm K, Burke T, Hofer H (2008) Do female hyaenas choose mates based on tenure? Reply to Van Horn et al. Nature 454: E2.

Höner OP, WachterB, EastML, StreichWJ, WilhelmK, Burke T, Hofer H (2007) Female mate choice drives the evolution of male-biased dispersal in a social mammal. Nature 448: 798-801.

Nagy M, Heckel G, Voigt CC, Mayer F (2007) Female-biased dispersal and patrilocal kin groups in a mammal with resource-defence polygyny. Proc R Soc Lond B 274: 3019-3025.