Evolution of a co-expression network involved in primate brain functions: clues to the evolution of human specific cognitive abilities
Author(s): Nowick, K, Berto, S
Cognitive abilities are among the most striking differences between humans and other primates. As cognition is a complex trait it is beneficial to analyze its evolution on multiple levels. Here we analyzed genome wide expression data of several human, chimpanzee, and rhesus macaque brains to identify molecular changes that may underlie the evolution of human-specific cognitive skills. Because transcription factors (TFs) are main players in regulating gene expression, we focused on TF changes that might drive expression pattern differences between the species. For each TF with a species-specific expression level we identified co-expressed genes, which are potential target genes or interaction partners of the respective TFs. Using this information we derived weighted topological overlap (wTO) networks in which the nodes are the TFs and the weighted links represent the commonality of the TFs’ co-expressed genes. We revealed: 1. The ancestral network, consisting only of links common to all three species, was involved in cognitive functions, such as forebrain development, synaptic plasticity, and learning, as inferred from the Gene Ontology (GO) terms enriched among the genes co-expressed with the most TFs in this network. 2. In the human network, TFs are more interconnected than in the chimpanzee and rhesus macaque network, indicating more complex regulation of genes involved in cognition in the human brain. 3. The TF sub-network constructed only from genes with a human-specific expression change was enriched for GO terms that point to changes in energy metabolism, learning and memory processes in the human brain. Moreover, only in this sub-network, but not in the sub-networks of the other species, we identified an excess of TFs implicated in mental disorders. Taken together, in a network of TFs that is predicted to regulate cognitive functions we identified evolutionary changes that are potentially involved in the evolution of human- specific cognitive abilities.
School of Biology
Experimental studies of human social learning strategies: exploring sex differences
Author(s): Cross, C, Brown, G, Morgan, T, Laland, K
Objectives Culture is an important driver of recent biological evolution in humans. The mechanisms by which information is transmitted between individuals can be studied at the population level – by cultural evolutionists, and at the individual level – by social psychologists. We combined methods from these two approaches to investigate how sex differences in confidence might lead to sex differences in the use of a copy-when-uncertain social learning strategy. Methods Participants (Study 1: N=97; Study 2: N=89) completed a series of two-alternative forced-choice puzzles and reported their confidence in each answer. They then saw the decisions of some previous participants before being asked again for their answer. Social information use was inferred when participants switched their answer to match that of the majority. We modelled the probability of social information use with participant sex, confidence in initial decision, and accuracy of initial decision as predictors. Results Across both studies, confidence had a large effect on social information use, indicative of a copy-when-uncertain strategy. Accuracy predicted confidence, indicating that this strategy is adaptive. Confidence also differed by sex: women reported lower confidence (independent of any small sex differences in accuracy), which in turn increased their probability of using social information. Conclusions Although both sexes appear to use a ‘copy-when-uncertain’ strategy, women are more likely to feel uncertain. This means that a strategy observed to be used in a population (e.g. copy-when-uncertain) can vary according to individual differences in psychological traits. Further integration of these two levels of explanation is therefore needed.
Institute of Evolutionary Biology and Environmental Studies
Fitness meets fitness: taking an evolutionary approach to physical fitness in humans
Author(s): Postma, E
Evolutionary biologists are usually the first to emphasize that Darwinian fitness has little in common with the meaning that is commonly attached to fitness by the general public, that is physical fitness. However, recent studies in humans and non-human animals are suggestive of an important role for physical fitness in shaping variation in Darwinian fitness via natural and sexual selection, both in the past and in the present. Indeed, it has been argued that it is selection on physical performance that has made us who we are today. To gain a better understanding of variation in (physical) fitness, I use concepts and methods from evolutionary biology and life-history theory and apply these to data on human running performance. Specifically, using a large (longitudinal and cross-sectional) data set for running performance by both men and women over a wide range of distances, I test for sex differences, the effects of ageing and training, and for trade-offs between long- versus short-distance and generalists versus specialists. I will use these findings to infer the selective pressures acting on physical fitness in humans, and to argue that Darwinian and physical fitness may have more in common with each other than is often assumed.
Institute of Integrative Biology & Department of Aquatic Ecology
Genetic constraints underlying human reproductive timing in a pre-modern Swiss village
Author(s): Bürkli, A, Postma, E
The trade-off between reproductive investment in early versus late life is central to life-history theory. Despite abundant empirical evidence in support of different versions of this trade-off, the specific trade-off between age at first reproduction (AFR) and age at last reproduction (ALR) has received little attention, especially in long-lived species with a pronounced reproductive senescence such as humans. Using genealogical data for a 19th-century Swiss village, we (i) quantify natural selection on reproductive timing, (ii) estimate additive genetic (co)variances, and (iii) use these to predict evolutionary responses. Selection gradients were computed using multiple linear regressions, and the additive genetic variance-covariance matrix was estimated using a restricted maximum-likelihood animal model. We found strong selection for both an early AFR and a late ALR, which resulted from selection for an earlier and longer reproductive period (RP, i.e. ALR-AFR). Furthermore, postponing AFR shortened RP in both sexes, but twice as much in women. Finally, AFR and ALR were strongly and positively genetically correlated, which led to a considerable reduction in the predicted responses to selection, or even rendered them maladaptive. These results provide evidence for strong genetic constraints underlying reproductive timing in humans, which may have contributed to the evolution of menopause.
Multiple instances of ancient balancing selection shared between humans and chimpanzees
Author(s): Leffler, EM, Gao, Z, Pfeifer, S, Ségurel, L, Auton, A, Venn, O, Bowden, R, Bontrop, R, Wall, JD, Sella, G, Donnelly, P, McVean, G, Przeworski, M
Balancing selection, in which two or more alleles are maintained in a population by selection, is predicted to lead to high diversity and to haplotypes with deep coalescence times. Moreover, if selection pressures are older than species split times, species may share alleles identically by descent. Such balanced polymorphisms are thought to be extremely rare, with a few notable examples involved in host immunity, such as at the MHC in primates and R genes in plants. However, modeling suggests that the footprint of balancing selection may be difficult to detect. Using genome-wide sequence data for 10 Western chimpanzees from the PanMap project and 1000 Genomes Pilot 1 data, we undertook a genome-wide search for orthologous sites polymorphic for the same alleles in both chimpanzee and human. We found that SNPs are shared in excess of what is expected by chance after accounting for local variation in the mutation rate. While it is difficult to distinguish balanced polymorphism from recurrent mutation for a single SNP, the short ancestral segments on which a balanced polymorphism resides may contain additional shared ancestral polymorphisms. We therefore focused on cases of two or more shared SNPs in close proximity and with the same LD patterns in both species, a scenario that is unlikely to occur by recurrent mutation. Besides the MHC, we identified 125 candidate loci, only two of which overlap exons. Notably, nearby genes are enriched for membrane glycoproteins, which are often found at host-pathogen interfaces. For five of the loci, more than two pairs of SNPs are shared with the same LD pattern and a phylogenetic tree clusters by haplotype rather than by species, providing strong evidence that the polymorphisms are ancestral and pointing to new targets of selection. These results suggest that balancing selection has acted on regulatory variation in both humans and chimpanzees and that pathogens may be a common pressure leading to such long-term balancing selection.
NZ Institute for Advanced Study
The Value of Reputation
Author(s): Pfeiffer, T, Tran, L, Krumme, C, Rand, DG
Reputation plays an important role in fostering human cooperation. A distinctive feature of reputation-based mechanisms is their capability to maintain cooperation among strangers engaged in one-shot interactions. In evolutionary biology, reputation provides a fascinating alternative to direct reciprocity, group selection or interactions between relatives for explaining the evolution of altruistic behavior. In the social sciences, reputation is of interest because one-shot interactions in global and electronic markets are more and more replacing traditional, repeated interactions within long-lasting communities. Empirical and theoretical work from both fields indicates that a good reputation is valuable in that it increases one’s expected payoff in future interactions. Here we present laboratory experiments for quantifying the value that participants place on a good reputation. To do so, we couple a Prisoner’s Dilemma (PD) game where participants can earn a good reputation with a market where reputation can be bought and sold. We show that the more valuable a good reputation is in the PD game, the higher are the prices at which it is traded in the market, suggesting that participants can assess the value of a good reputation. We also find that in the presence of trading, cooperation is maintained at a lower level then in the absence of trading. This suggests that trading of reputation can have a detrimental effect on cooperation, perhaps through “crowding out” of the participants’ intrinsic motivation to cooperate. However, our experiments also demonstrate that trading of reputation can promote cooperation. When participants play a short fixed-length series of Prisoner’s Dilemmas, the opportunity to sell good reputation when exiting the game can mitigate end-game effects. Thus reputation markets could potentially create value and increase social welfare when applied in an appropriate context.
Department of Evolutionary Genetics
The demographic transition influences variance in fitness and selection on height and BMI in rural Gambia
Author(s): Courtiol, A
Recent human history is marked by demographic transitions characterized by declines in mortality and fertility. By influencing the variance in those fitness components, demographic transitions can affect selection on other traits. Parallel to changes in selection triggered by demography per se, relationships between fitness and anthropometric traits are also expected to change due to modification of the environment. Here we explore for the first time these two main evolutionary consequences of demographic transitions using a unique data set containing survival, fertility, and anthropometric data for thousands of women in rural Gambia from 1956–2010. We show how the demographic transition influenced directional selection on height and body mass index (BMI). We observed a change in selection for both traits mediated by variation in fertility: selection initially favored short females with high BMI values but shifted across the demographic transition to favor tall females with low BMI values. We demonstrate that these differences resulted both from changes in fitness variance that shape the strength of selection and from shifts in selective pressures triggered by environmental changes. These results suggest that demographic and environmental trends encountered by current human populations worldwide are likely to modify, but not stop, natural selection in humans.
Department of Biosciences
Why is childbirth so hard in humans?
Author(s): Fischer, B
Compared to other primates, childbirth is remarkably difficult in humans, the reason being that the head of the human fetus is large in comparison to the birth-relevant dimensions of the human pelvis. Modern human pelvic morphology must serve more than one purpose: It is thought to have evolved as a compromise between being shaped for upright walking and giving birth to large-headed neonates. This “obstetric dilemma” arose as a consequence of bipedal humans evolving increasingly larger brains. Although anatomically modern humans have existed for at least 100,000 years, and although the selection pressure for evolving wider birth canals has probably been considerable throughout, we do not see any evolutionary response in birth-relevant pelvic dimensions. We hypothesize that this lack of response is due to evolutionary constraints that inhibit the evolution of wider birth canals in humans. In this study we try to identify allometric constraints using morphometric techniques on a human skeletal sample.