Dieter Lukas

The Evolution of Social Monogamy in Mammals

The Only Flame in Town Unusual for mammals, humans are notably socially monogamous, with pair bonding sometimes lasting decades. Why? Lukas and Clutton-Brock (p. 526; see the Perspective by Kappeler) examined data from over 2500 mammalian species across 26 orders containing 60 evolutionary transitions to monogamy. In every case, the ancestral condition was one where females were solitary and where male infanticide was unusual. Monogamy appears to arise not as a response to a need for paternal care, but largely as a mate-guarding strategy. Social monogamy developed in mammalian species where males could not defend access to multiple females. [Also see Perspective by Kappeler] The evolution of social monogamy has intrigued biologists for over a century. Here, we show that the ancestral condition for all mammalian groups is of solitary individuals and that social monogamy is derived almost exclusively from this social system. The evolution of social monogamy does not appear to have been associated with a high risk of male infanticide, and paternal care is a consequence rather than a cause of social monogamy. Social monogamy has evolved in nonhuman mammals where breeding females are intolerant of each other and female density is low, suggesting that it represents a mating strategy that has developed where males are unable to defend access to multiple females.

Cooperative breeding and monogamy in mammalian societies

Comparative studies of social insects and birds show that the evolution of cooperative and eusocial breeding systems has been confined to species where females mate completely or almost exclusively with a single male, indicating that high levels of average kinship between group members are necessary for the evolution of reproductive altruism. In this paper, we show that in mammals, the evolution of cooperative breeding has been restricted to socially monogamous species which currently represent 5 per cent of all mammalian species. Since extra-pair paternity is relatively uncommon in socially monogamous and cooperatively breeding mammals, our analyses support the suggestion that high levels of average kinship between group members have played an important role in the evolution of cooperative breeding in non-human mammals, as well as in birds and insects.

The evolution of social philopatry and dispersal in female mammals

In most social mammals, some females disperse from their natal group while others remain and breed there throughout their lives but, in a few, females typically disperse after adolescence and few individuals remain and breed in their natal group. These contrasts in philopatry and dispersal have an important consequence on the kinship structure of groups which, in turn, affects forms of social relationships between females. As yet, there is still widespread disagreement over the reasons for the evolution of habitual female dispersal, partly as a result of contrasting definitions of dispersal. This paper reviews variation in the frequency with which females leave their natal group or range (social dispersal) and argues that both the avoidance of local competition for resources and breeding opportunities and the need to find unrelated partners play an important role in contrasts between and within species.

Individual variation in cognitive performance: developmental and evolutionary perspectives

Animal cognition experiments frequently reveal striking individual variation but rarely consider its causes and largely ignore its potential consequences. Studies often focus on a subset of high-performing subjects, sometimes viewing evidence from a single individual as sufficient to demonstrate the cognitive capacity of a species. We argue that the emphasis on demonstrating species-level cognitive capacities detracts from the value of individual variation in understanding cognitive development and evolution. We consider developmental and evolutionary interpretations of individual variation and use meta-analyses of data from published studies to examine predictors of individual performance. We show that reliance on small sample sizes precludes robust conclusions about individual abilities as well as inter- and intraspecific differences. We advocate standardization of experimental protocols and pooling of data between laboratories to improve statistical rigour. Our analyses show that cognitive performance is influenced by age, sex, rearing conditions and previous experience. These effects limit the validity of comparative analyses unless developmental histories are taken into account, and complicate attempts to understand how cognitive traits are expressed and selected under natural conditions. Further understanding of cognitive evolution requires efforts to elucidate the heritability of cognitive traits and establish whether elevated cognitive performance confers fitness advantages in nature.

To what extent does living in a group mean living with kin

Chimpanzees live in large groups featuring remarkable levels of gregariousness and cooperation among the males. Because males stay in their natal communities their entire lives and are hence expected to be living with male relatives, cooperation is therefore assumed to occur within one large ‘family’ group. However, we found that the average relatedness among males within several chimpanzee groups as determined by microsatellite analysis is in fact rather low, and only rarely significantly higher than average relatedness of females in the groups or of males compared across groups. To explain these findings, mathematical predictions for average relatedness according to group size, reproductive skew and sex bias in dispersal were derived. The results show that high average relatedness among the philopatric sex is only expected in very small groups, which is confirmed by a comparison with published data. Our study therefore suggests that interactions among larger number of individuals may not be primarily driven by kin relationships.

Y‐chromosome analysis confirms highly sex‐biased dispersal and suggests a low male effective population size in bonobos (Pan paniscus)

Dispersal is a rare event that is difficult to observe in slowly maturing, long‐lived wild animal species such as the bonobo. In this study we used sex‐linked (mitochondrial DNA sequence and Y‐chromosome microsatellite) markers from the same set of individuals to estimate the magnitude of difference in effective dispersal between the sexes and to investigate the long‐term demographic history of bonobos. We sampled 34 males from four distinct geographical areas across the bonobo distribution range. As predicted for a female‐dispersing species, we found much higher levels of differentiation among local bonobo populations based upon Y‐chromosomal than mtDNA genetic variation. Specifically, almost all of the Y‐chromosomal variation distinguished populations, while nearly all of the mtDNA variation was shared between populations. Furthermore, genetic distance correlated with geographical distance for mtDNA but not for the Y chromosome. Female bonobos have a much higher migration rate and/or effective population size as compared to males, and the estimate for the mitochondrial TMRCA (time to most recent common ancestor) was approximately 10 times greater than the estimate for the Y chromosome (410 000 vs. 40 000–45 000). For humans the difference is merely a factor of two, suggesting a more stable demographic history in bonobos in comparison to humans.

Nuclear insertions help and hinder inference of the evolutionary history of gorilla mtDNA.

Numts are fragments of mitochondrial DNA (mtDNA) that have been translocated to the nucleus, where they can persist while their mitochondrial counterparts continue to rapidly evolve. Thus, numts represent ‘molecular fossils’ useful for comparison with mitochondrial variation, and are particularly suited for studies of the fast‐evolving hypervariable segment of the mitochondrial control region (HV1). Here we used information from numts found in western gorillas (Gorilla gorilla) and eastern gorillas (Gorilla beringei) to estimate that these two species diverged about 1.3 million years ago (Ma), an estimate similar to recent calculations for the divergence of chimpanzee and bonobo. We also describe the sequence of a gorilla numt still possessing a segment lost from all contemporary gorilla mtDNAs. In contrast to that sequence, many numts of the HV1 are highly similar to authentic mitochondrial organellar sequences, making it difficult to determine whether purported mitochondrial sequences truly derive from that genome. We used all available organellar HV1 and corresponding numt sequences from gorillas in a phylogenetic analysis aimed at distinguishing these two types of sequences. Numts were found in several clades in the tree. This, in combination with the fact that only a limited amount of the extant variation in gorillas has been sampled, suggests that categorization of new sequences by the indirect means of phylogenetic comparison would be prone to uncertainty. We conclude that for taxa such as gorillas that contain numerous numts, direct approaches to the authentication of HV1 sequences, such as amplification strategies relying upon the circularity of the mtDNA molecule, remain necessary.

The evolution of infanticide by males in mammalian societies

Male mammals often kill conspecific offspring. The benefits of such infanticide to males, and its costs to females, probably vary across mammalian social and mating systems. We used comparative analyses to show that infanticide primarily evolves in social mammals in which reproduction is monopolized by a minority of males. It has not promoted social counterstrategies such as female gregariousness, pair living, or changes in group size and sex ratio, but is successfully prevented by female sexual promiscuity, a paternity dilution strategy. These findings indicate that infanticide is a consequence, rather than a cause, of contrasts in mammalian social systems affecting the intensity of sexual conflict. Field data from 260 mammalian species suggest that males killing young is an evolutionary consequence of sexual conflict. Why some male animals kill infants One of the most unpleasant aspects of social life in some animal species is killing of the young by adult males. Lukas and Huchard looked at mammalian groups with a variety of social systems—from mice to mongoose and from bats to bears. Infanticidal behavior in males appeared to be a result of sexual conflict in social species with nonseasonal breeding. Killing of a females young by a new male will speed her return to a reproductive state and allow him to raise his own young. Evolutionarily, the only successful defense in females appears to be polyandry: Females that mate with multiple males make it hard for any one male to know that he is, or is not, the father of her offspring. Science, this issue p. 841

Major histocompatibility complex and microsatellite variation in two populations of wild gorillas

In comparison to their close relatives the chimpanzees and humans, very little is known concerning the amount and structure of genetic variation in gorillas. Two species of gorillas are recognized and while the western gorillas number in the tens of thousands, only several hundred representatives of the mountain gorilla subspecies of eastern gorillas survive. To analyse the possible effects of these different population sizes, this study compares the variation observed at microsatellite and major histocompatibility complex (MHC) loci in samples of wild western and mountain gorillas, collected using a sampling scheme that targeted multiple social groups within defined geographical areas. Noninvasive samples proved a viable source of DNA for sequence analysis of the second exon of the DRB loci of the MHC. Observed levels of variation at the MHC locus were similar between the two gorilla species and were comparable to those in other primates. Comparison of results from analysis of variation at multiple microsatellite loci found only a slight reduction in heterozygosity for the mountain gorillas despite the relatively smaller population size.

Life histories and the evolution of cooperative breeding in mammals

While the evolution of cooperative breeding systems (where non-breeding helpers participate in rearing young produced by dominant females) has been restricted to lineages with socially monogamous mating systems where coefficients of relatedness between group members are usually high, not all monogamous lineages have produced species with cooperative breeding systems, suggesting that other factors constrain the evolution of cooperative breeding. Previous studies have suggested that life-history parameters, including longevity, may constrain the evolution of cooperative breeding. Here, we show that transitions to cooperative breeding across the mammalian phylogeny have been restricted to lineages where females produce multiple offspring per birth. We find no support for effects of longevity or of other life-history parameters. We suggest that the evolution of cooperative breeding has been restricted to monogamous lineages where helpers have the potential to increase the reproductive output of breeders.