Alexei A. Maklakov

Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain.

Summary The large variation in brain size that exists in the animal kingdom has been suggested to have evolved through the balance between selective advantages of greater cognitive ability and the prohibitively high energy demands of a larger brain (the “expensive-tissue hypothesis” [1]). Despite over a century of research on the evolution of brain size, empirical support for the trade-off between cognitive ability and energetic costs is based exclusively on correlative evidence [2], and the theory remains controversial [3, 4]. Here we provide experimental evidence for costs and benefits of increased brain size. We used artificial selection for large and small brain size relative to body size in a live-bearing fish, the guppy (Poecilia reticulata), and found that relative brain size evolved rapidly in response to divergent selection in both sexes. Large-brained females outperformed small-brained females in a numerical learning assay designed to test cognitive ability. Moreover, large-brained lines, especially males, developed smaller guts, as predicted by the expensive-tissue hypothesis [1], and produced fewer offspring. We propose that the evolution of brain size is mediated by a functional trade-off between increased cognitive ability and reproductive performance and discuss the implications of these findings for vertebrate brain evolution.

THE TRANSITION TO SOCIAL INBRED MATING SYSTEMS IN SPIDERS: ROLE OF INBREEDING TOLERANCE IN A SUBSOCIAL PREDECESSOR

Abstract The social spiders are unusual among cooperatively breeding animals in being highly inbred. In contrast, most other social organisms are outbred owing to inbreeding avoidance mechanisms. The social spiders appear to originate from solitary subsocial ancestors, implying a transition from outbreeding to inbreeding mating systems. Such a transition may be constrained by inbreeding avoidance tactics or fitness loss due to inbreeding depression. We examined whether the mating system of a subsocial spider, in a genus with three social congeners, is likely to facilitate or hinder the transition to inbreeding social systems. Populations of subsocial Stegodyphus lineatus are substructured and spiders occur in patches, which may consist of kin groups. We investigated whether male mating dispersal prevents matings within kin groups in natural populations. Approximately half of the marked males that were recovered made short moves (< 5m) and mated within their natal patch. This potential for inbreeding was counterbalanced by a relatively high proportion of immigrant males. In mating experiments, we tested whether inbreeding actually results in lower offspring fitness. Two levels of inbreeding were tested: full sibling versus non-sib matings and matings of individuals within and between naturally occurring patches of spiders. Neither full siblings nor patch mates were discriminated against as mates. Sibling matings had no effect on direct fitness traits such as fecundity, hatching success, time to hatching and survival of the offspring, but negatively affected offspring growth rates and adult body size of both males and females. Neither direct nor indirect fitness measures differed significantly between within patch and between-patch pairs. We tested the relatedness between patch mates and nonpatch mates using DNA fingerprinting (TE-AFLP). Kinship explained 30% of the genetic variation among patches, confirming that patches are often composed of kin. Overall, we found limited male dispersal, lack of kin discrimination, and tolerance to low levels of inbreeding. These results suggest a history of inbreeding which may reduce the frequency of deleterious recessive alleles in the population and promote the evolution of inbreeding tolerance. It is likely that the lack of inbreeding avoidance in subsocial predecessors has facilitated the transition to regular inbreeding social systems.

Longer Life Span Evolves under High Rates of Condition-Dependent Mortality

Aging affects nearly all organisms, but how aging evolves is still unclear. The central prediction of classic theory is that high extrinsic mortality leads to accelerated aging and shorter intrinsic life span. However, this prediction considers mortality as a random process, whereas mortality in nature is likely to be condition dependent. Therefore, the novel theory maintains that condition dependence may dramatically alter, and even reverse, the classic pattern. We present experimental evidence for the evolution of longer life span under high condition-dependent mortality. We employed an experimental evolution design, using a nematode, Caenorhabditis remanei, that allowed us to disentangle the effects of mortality rate (high versus low) and mortality source (random versus condition dependent). We observed the evolution of shorter life span under high random mortality, confirming the classic prediction. In contrast, high condition-dependent mortality led to the evolution of longer life span, supporting a key role of condition dependence in the evolution of aging. This life-span extension was not the result of a trade-off with reproduction. By simultaneously corroborating the classic results [8-10] and providing the first experimental evidence for the novel theory, our study resolves apparent contradictions in the study of aging and challenges the traditional paradigm by demonstrating that condition-environment interactions dictate the evolutionary trajectory of aging.

Brains and the city: big-brained passerine birds succeed in urban environments

Urban regions are among the most human-altered environments on Earth and they are poised for rapid expansion following population growth and migration. Identifying the biological traits that determine which species are likely to succeed in urbanized habitats is important for predicting global trends in biodiversity. We provide the first evidence for the intuitive yet untested hypothesis that relative brain size is a key factor predisposing animals to successful establishment in cities. We apply phylogenetic mixed modelling in a Bayesian framework to show that passerine species that succeed in colonizing at least one of 12 European cities are more likely to belong to big-brained lineages than species avoiding these urban areas. These data support findings linking relative brain size with the ability to persist in novel and changing environments in vertebrate populations, and have important implications for our understanding of recent trends in biodiversity.

Survival benefits select for group living in a social spider despite reproductive costs

The evolution of cooperation requires benefits of group living to exceed costs. Hence, some components of fitness are expected to increase with increasing group size, whereas others may decrease because of competition among group members. The social spiders provide an excellent system to investigate the costs and benefits of group living: they occur in groups of various sizes and individuals are relatively short‐lived, therefore life history traits and Lifetime Reproductive Success (LRS) can be estimated as a function of group size. Sociality in spiders has originated repeatedly in phylogenetically distant families and appears to be accompanied by a transition to a system of continuous intra‐colony mating and extreme inbreeding. The benefits of group living in such systems should therefore be substantial. We investigated the effect of group size on fitness components of reproduction and survival in the social spider Stegodyphus dumicola in two populations in Namibia. In both populations, the major benefit of group living was improved survival of colonies and late‐instar juveniles with increasing colony size. By contrast, female fecundity, female body size and early juvenile survival decreased with increasing group size. Mean individual fitness, estimated as LRS and calculated from five components of reproduction and survival, was maximized for intermediate‐ to large‐sized colonies. Group living in these spiders thus entails a net reproductive cost, presumably because of an increase in intra‐colony competition with group size. This cost is traded off against survival benefits at the colony level, which appear to be the major factor favouring group living. In the field, many colonies occur at smaller size than expected from the fitness curve, suggesting ecological or life history constraints on colony persistence which results in a transient population of relatively small colonies.

National income inequality predicts women's preferences for masculinized faces better than health does

In their paper ‘The health of a nation predicts their mate preferences’, DeBruine et al. [[1][1]] find that womens preferences for facial masculinity from a large, cross-cultural sample of individuals from developed countries is negatively correlated with a composite National Health Index (NHI

EVOLUTION OF MALE AND FEMALE GENITALIA FOLLOWING RELEASE FROM SEXUAL SELECTION

Despite the key functions of the genitalia in sexual interactions and fertilization, the role of sexual selection and conflict in shaping genital traits remains poorly understood. Seed beetle (Callosobruchus maculatus) males possess spines on the intromittent organ, and females possess a thickened reproductive tract wall that also bears spines. We investigated the role of sexual selection and conflict by imposing monogamous mating on eight replicate populations of this naturally polygamous insect, while maintaining eight other populations under polygamy. To establish whether responses to mating system manipulation were robust to ecological context, we simultaneously manipulated life‐history selection (early/late reproduction). Over 18–21 generations, male genital spines evolved relatively reduced length in large males (i.e., shallower static allometry) in monogamous populations. Two nonintromittent male genital appendages also evolved in response to the interaction of mating system and ecology. In contrast, no detectable evolution occurred in female genitalia, consistent with the expectation of a delayed response in defensive traits. Our results support a sexually antagonistic role for the male genital spines, and demonstrate the evolution of static allometry in response to variation in sexual selection opportunity. We argue that further advances in the study of genital coevolution will require a much more detailed understanding of the functions of male and female genital traits.

Sexual conflict in the wild : Elevated mating rate reduces female lifetime reproductive success

Sexual conflict over mating rate is suggested to play a pivotal role in male‐female coevolution, and females are predicted to reject superfluous mating attempts. Recent work suggests that direct effects of multiple mating on female fitness are not fully understood. A major concern in studies of sexual conflict is how well the data obtained under controlled laboratory settings relate to natural conditions. We tested the effect of female multiple mating on reproductive success in a natural population of a polyandrous spider, Stegodyphus lineatus. Previous studies show that a male who succeeds in entering a female nest also mates with her; therefore, we used male encounter rate as a proxy of female mating rate. We further elevated female mating rate by introducing males into females’ nests. Female lifetime reproductive success was assessed as the likelihood of successful reproduction, offspring production, and juvenile offspring body mass. Increased mating rate increased the time to oviposition and reduced the likelihood of successful reproduction. Female mating rate negatively affected offspring body mass. Manipulated females produced fewer offspring than control females. The observed patterns imply a net cost of polyandry to females and suggest that natural mating rates can be suboptimal for females under natural conditions.

Sex differences in the genetic architecture of lifespan in a seed beetle : extreme inbreeding extends male lifespan

BackgroundSex differences in lifespan are ubiquitous throughout the animal kingdom but the causes underlying this phenomenon remain poorly understood. Several explanations based on asymmetrical inheritance patterns (sex chromosomes or mitochondrial DNA) have been proposed, but these ideas have rarely been tested experimentally. Alternatively, sexual dimorphism in lifespan could result from sex-specific selection, caused by fundamental differences in how males and females optimize their fitness by allocating resources into current and future reproduction.ResultsHere we used sex-specific responses to inbreeding to study the genetic architecture of lifespan and mortality rates in Callosobruchus maculatus, a seed beetle that shows sexual dimorphism in lifespan. Two independent assays revealed opposing sex-specific responses to inbreeding. The combined data set showed that inbred males live longer than outbred males, while females show the opposite pattern. Both sexes suffered reduced fitness measured as lifetime reproductive success as a result of inbreeding.ConclusionNo model based on asymmetrical inheritance can explain increased male lifespan in response to inbreeding. Our results are however compatible with models based on sex-specific selection on reproductive strategies. We therefore suggest that sex-specific differences in lifespan in this species primarily result from sexually divergent selection.

Sexual selection for increased male body size and protandry in a spider

Female-biased sexual size dimorphism (SSD) is found in many organisms yet is poorly understood. Spiders in general, and web-building species in particular, typically have strongly female-biased SSD. We investigated the causes of SSD in the web-building spider Stegodyphus lineatus. Females are slightly, but significantly, larger than males. Large females are more fecund but the selection pressures on male body size are not clear. Males were introduced on to the webs of virgin and mated females and we also conducted competition experiments between males. Large males did not have longer copulations, nor did they mate more successfully with virgin females than small males did; however, they were more successful with previously mated females and remated more often. They also won more fights, and were more successful at obtaining prey from the females web. Indiscriminate mating by virgin females, however, conferred a fitness advantage on early maturing males. We suggest that the females mating strategy selects for protandry, which results in female-biased SSD, despite the selection for large body size in males. Indiscriminate mating by females and a trade-off between time to maturation and male body size may be important in understanding the evolution of female-biased SSD.