Fitness and Power: The Contribution of Genetics to the History of Differential Reproduction

Textual evidence from pre-modern societies supports the prediction that status differences among men translate to variance in reproductive success. In recent years, analysis of genetic data has opened up new ways of studying this relationship. By investigating cases that range over several millennia, these analyses repeatedly document the replacement of local men by newcomers and reveal instances of exceptional reproductive success of specific male lineages. These findings suggest that violent population transfers and conquests could generate considerable reproductive advantages for male dominants. At the same time, this does not always seem to have been the case. Moreover, it is difficult to link such outcomes to particular historical characters or events, or to identify status-biased reproductive inequalities within dominant groups. The proximate factors that mediated implied imbalances in reproductive success often remain unclear. A better understanding of the complex interplay between social power and genetic fitness will only arise from sustained transdisciplinary engagement.

How accurately do behavioural observations predict reproductive success in free-ranging lizards?

Behavioural ecologists often use data on patterns of male–female association to infer reproductive success of free-ranging animals. For example, a male seen with several females during the mating season is predicted to father more offspring than a male not seen with any females. We explored the putative correlation between this behaviour and actual paternity (as revealed by microsatellite data) from a long-term study on sand lizards ( Lacerta agilis ), including behavioural observations of 574 adult males and 289 adult females, and paternity assignment of more than 2500 offspring during 1998–2007. The number of males that contributed paternity to a female's clutch was correlated with the number of males seen accompanying her in the field, but not with the number of copulation scars on her body. The number of females that a male accompanied in the field predicted the number of females with whom he fathered offspring, and his annual reproductive success (number of progeny). Although behavioural data explained less than one-third of total variance in reproductive success, our analysis supports the utility of behavioural-ecology studies for predicting paternity in free-ranging reptiles.

How convincing is a matching Y-chromosome profile?

The introduction of forensic autosomal DNA profiles was controversial, but the problems were successfully addressed, and DNA profiling has gone on to revolutionise forensic science. Y-chromosome profiles are valuable when there is a mixture of male-source and female-source DNA, and interest centres on the identity of the male source(s) of the DNA. The problem of evaluating evidential weight is even more challenging for Y profiles than for autosomal profiles. Numerous approaches have been proposed, but they fail to deal adequately with the fact that men with matching Y-profiles are re-lated in extended patrilineal clans, many of which may not be represented in available databases. This problem has been exacerbated by recent profiling kits with high mutation rates. Because the relevant population is difficult to define, yet the number of matching relatives is fixed as population size varies, it is typically infeasible to derive population-based match probabilities relevant to a specific crime. We propose a conceptually simple solution, based on a simulation model and software to approximate the distribution of the number of males with a matching Y profile. We show that this distribution is robust to different values for the variance in reproductive success and the population growth rate. We also use importance sampling reweighting to derive the distribution of the number of matching males conditional on a database frequency, finding that this conditioning typically has only a modest impact. We illustrate the use of our approach to quantify the value of Y profile evidence for a court in a way that is both scientifically valid and easily comprehensible by a judge or juror.

Intra-sexual selection in cooperative mammals and birds: why are females not bigger and better armed?

In cooperatively breeding mammals and birds, intra-sexual reproductive competition among females may often render variance in reproductive success higher among females than males, leading to the prediction that intra-sexual selection in such species may have yielded the differential exaggeration of competitive traits among females. However, evidence to date suggests that female-biased reproductive variance in such species is rarely accompanied by female-biased sexual dimorphisms. We illustrate the problem with data from wild Damaraland mole-rat, Fukomys damarensis , societies: the variance in lifetime reproductive success among females appears to be higher than that among males, yet males grow faster, are much heavier as adults and sport larger skulls and incisors (the weapons used for fighting) for their body lengths than females, suggesting that intra-sexual selection has nevertheless acted more strongly on the competitive traits of males. We then consider potentially general mechanisms that could explain these disparities by tempering the relative intensity of selection for competitive trait exaggeration among females in cooperative breeders. Key among these may be interactions with kin selection that could nevertheless render the variance in inclusive fitness lower among females than males, and fundamental aspects of the reproductive biology of females that may leave reproductive conflict among females more readily resolved without overt physical contests.

Sexual selection and hermaphroditic organisms: Testing theory

Sexual selection is widespread if not ubiquitous in hermaphroditic organisms. Although many phenomena that have been described as sexual selection in gonochores, (e.g. harem polygamy, multiple mating, elaborate courtship, even secondary sexual characters) can be found in some hermaphrodites, what is more interesting is the ways in which sexual selection in hermaphrodites may differ from dioecious taxa. In hermaphrodites, an individual’s mating success includes its success from both sexual roles. Secondly, in many simultaneously hermaphroditic taxa there is strong evidence of sexual selection and yet the operational sex ratio is 1:1, by definition. Many simultaneous hermaphrodites have elaborate courtship and genital anatomy, suggesting sexual selection plays an important role in reproductive success. Sperm competition and cryptic female choice mean that the number of mates acquired is not necessarily a predictor of reproductive success. Even in simultaneous hermaphrodites with reciprocal mating, variance in reproductive success through the male role and through the female role may differ in a population. Moreover hermaphrodites may choose to emphasize one sexual role over the other. Data suggest that the preferred role varies in hermaphrodites, which creates an opportunity to test fundamental predictions and assumptions of sexual selection theory. Hermaphrodites may vary their emphasis on one sexual role over the other either developmentally or behaviorally in response to environmental or social parameters. How they use this capability in acquiring more or higher quality mates still requires study.

Beyond promiscuity: mate-choice commitments in social breeding

Obligate eusociality with distinct caste phenotypes has evolved from strictly monogamous sub-social ancestors in ants, some bees, some wasps and some termites. This implies that no lineage reached the most advanced form of social breeding, unless helpers at the nest gained indirect fitness values via siblings that were identical to direct fitness via offspring. The complete lack of re-mating promiscuity equalizes sex-specific variances in reproductive success. Later, evolutionary developments towards multiple queen-mating retained lifetime commitment between sexual partners, but reduced male variance in reproductive success relative to female's, similar to the most advanced vertebrate cooperative breeders. Here, I (i) discuss some of the unique and highly peculiar mating system adaptations of eusocial insects; (ii) address ambiguities that remained after earlier reviews and extend the monogamy logic to the evolution of soldier castes; (iii) evaluate the evidence for indirect fitness benefits driving the dynamics of (in)vertebrate cooperative breeding, while emphasizing the fundamental differences between obligate eusociality and cooperative breeding; (iv) infer that lifetime commitment is a major driver towards higher levels of organization in bodies, colonies and mutualisms. I argue that evolutionary informative definitions of social systems that separate direct and indirect fitness benefits facilitate transparency when testing inclusive fitness theory.