González-Forero M & Gardner A (2018) Inference of ecological and social drivers of human brain-size evolution. Nature 557, 554-557.

The human brain is unusually large. It has tripled in size from Australopithecines to modern humans and has become almost six times larger than expected for a placental mammal of human size. Brains incur high metabolic costs and accordingly a long-standing question is why the large human brain has evolved. The leading hypotheses propose benefits of improved cognition for overcoming ecological, social or cultural challenges. However, these hypotheses are typically assessed using correlative analyses, and establishing causes for brain-size evolution remains difficult. Here we introduce a metabolic approach that enables causal assessment of social hypotheses for brain-size evolution. Our approach yields quantitative predictions for brain and body size from formalized social hypotheses given empirical estimates of the metabolic costs of the brain. Our model predicts the evolution of adult Homo sapiens-sized brains and bodies when individuals face a combination of 60% ecological, 30% cooperative and 10% between-group competitive challenges, and suggests that between-individual competition has been unimportant for driving human brain-size evolution. Moreover, our model indicates that brain expansion in Homo was driven by ecological rather than social challenges, and was perhaps strongly promoted by culture. Our metabolic approach thus enables causal assessments that refine, refute and unify hypotheses of brain-size evolution.

Davies NG & Gardner A (2018) Monogamy promotes altruistic sterility in insect societies. Royal Society Open Science 55, 172190.

Monogamy is associated with sibling-directed altruism in multiple animal taxa, including insects, birds and mammals. Inclusive-fitness theory readily explains this pattern by identifying high relatedness as a promoter of altruism. In keeping with this prediction, monogamy should promote the evolution of voluntary sterility in insect societies if sterile workers make for better helpers. However, a recent mathematical population-genetics analysis failed to identify a consistent effect of monogamy on voluntary worker sterility. Here, we revisit that analysis. First, we relax genetic assumptions, considering not only alleles of extreme effect—encoding either no sterility or complete sterility—but also alleles with intermediate effects on worker sterility. Second, we broaden the stability analysis—which focused on the invasibility of populations where either all workers are fully sterile or all workers are fully reproductive—to identify where intermediate pure or mixed evolutionarily stable states may occur. Third, we consider a broader range of demographically explicit ecological scenarios relevant to altruistic worker non-reproduction and to the evolution of eusociality more generally. We find that, in the absence of genetic constraints, monogamy always promotes altruistic worker sterility and may inhibit spiteful worker sterility. Our extended analysis demonstrates that an exact population-genetics approach strongly supports the prediction of inclusive-fitness theory that monogamy promotes sib-directed altruism in social insects.

Faria GS, Varela SAM & Gardner A (2018) The relation between R. A. Fisher’s sexy-son hypothesis and W. D. Hamilton’s greenbeard effect. Evolution Letters. doi:10.1002/ev13.53

Recent years have seen a growing interest in the overlap between the theories of kin selection and sexual selection. One potential overlap is with regards to whether R. A. Fisher’s “sexy-son” hypothesis, concerning the evolution of extravagant sexual ornamentation, may be framed in terms of W. D. Hamilton’s greenbeard effect, concerning scenarios in which individuals carry an allele that allows them to recognize and behave differently toward other carriers of the same allele. Specifically, both scenarios involve individuals behaving differently toward social partners who exhibit a phenotypic marker, with linkage disequilibrium between marker and behavior loci ensuring genetic relatedness between actor and recipient at the behavior locus. However, the formal connections between the two theories remain unclear. Here, we develop these connections by: (1) asking what kind of greenbeard is involved in the sexy-son hypothesis; (2) exploring the relationship between the problem of “falsebeards” and the “lek paradox”; (3) investigating whether these two problems may be resolved in analogous ways; and (4) determining whether population structure facilitates both of these evolutionary phenomena. By building this conceptual bridge, we are able to import results from the field of kin selection to sexual selection, and vice versa, yielding new insights into both topics.

O’Brien S, Hesse E, Luján A, Hodgson D, Gardner A & Buckling A (in press) No effect of intraspecific relatedness on public goods cooperation in a complex community. Evolution.

Many organisms – notably microbes – are embedded within complex communities where cooperative behaviours in the form of excreted public goods can benefit other species. Under such circumstances, intraspecific interactions are likely to be less important in driving the evolution of cooperation. We first illustrate this idea with a simple theoretical model, showing that relatedness – the extent to which individuals with the same cooperative alleles interact with each other – has a reduced impact on the evolution of cooperation when public goods are shared between species. We test this empirically using strains of Pseudomonas aeruginosa that vary in their production of metal-chelating siderophores in copper contaminated compost (an interspecific public good). We show that non-siderophore producers grow poorly relative to producers under high relatedness, but this cost can be alleviated by the presence of the isogenic producer (low relatedness) and/or the compost microbial community. Hence, relatedness can become unimportant when public goods provide interspecific benefits.

Best R, Ruxton GD & Gardner A (in press) Intragroup and intragenomic conflict over chemical defence against predators. Ecology and Evolution doi: 10.1002/ece3.3926

Insects are often chemically defended against predators. There is considerable evidence for a group-beneficial element to their defenses, and an associated potential for individuals to curtail their own investment in costly defense while benefitting from the investments of others, termed “automimicry.” Although females in chemically defended taxa often lay their eggs in clusters, leading to siblings living in close proximity, current models of automimicry have neglected kin-selection effects, which may be expected to curb the evolution of such selfishness. Here, we develop a general theory of automimicry that explicitly incorporates kin selection. We investigate how female promiscuity modulates intragroup and intragenomic conflicts overinvestment into chemical defense, finding that individuals are favored to invest less than is optimal for their group, and that maternal-origin genes favor greater investment than do paternal-origin genes. We translate these conflicts into readily testable predictions concerning gene expression patterns and the phenotypic consequences of genomic perturbations, and discuss how our results may inform gene discovery in relation to economically important agricultural products.

Photo credit: Wikimedia

Cameron Turner has joined us as a Visiting PhD Student from ANU, he’ll be working in St Andrews during 2018 on models of social learning and cultural evolution. Welcome Cameron!

As part of an agreement with the Chinese Scholarship Council (CSC), the University of St Andrews is offering 30 fully-funded 4-year PhD studentships to Chinese nationals. Full details of the scheme are available here.

I offer projects on evolutionary theory, so if you are interested in pursuing this opportunity in my research group, please do get in touch. The deadline for applications is 19 Jan 2018.

Gardner A & Úbeda F (2017) The meaning of intragenomic conflict. Nature Ecology & Evolution doi: 10.1038/s41559-017-0354-9.

Recent years have seen an explosion of interest in genes that function for their own good and to the detriment of other genes that reside in the same genome. Such intragenomic conflicts are increasingly recognized to underpin maladaptation and disease. However, progress has been impeded by a lack of clear understanding regarding what intragenomic conflict actually means, and an associated obscurity concerning its fundamental drivers. Here we develop a general theory of intragenomic conflict in which genes are viewed as inclusive-fitness-maximizing agents that come into conflict when their inclusive-fitness interests disagree. This yields a classification of all intragenomic conflicts into three categories according to whether genes disagree about where they have come from, where they are going, or where they currently are. We illustrate each of these three basic categories, survey and classify all known forms of intragenomic conflict, and discuss the implications for organismal maladaptation and human disease.

Jasmeen Kanwal has joined us to undertake a postdoc on social evolution of digital organisms. Welcome to the group, Jasmeen!

Thomas Hitchcock has joined us to pursue a PhD in social evolution theory. Welcome to the group, Thomas!