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[New paper] Paternal genome elimination promotes altruism in viscous populations

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Hitchcock TJ & Gardner A (in press) Paternal genome elimination promotes altruism in viscous populations. Evolution https://doi.org/10.1111/evo.14585

Image: https://www.craiyon.com

Population viscosity has long been thought to promote the evolution of altruism. However, in the simplest scenarios, the potential for altruism is invariant with respect to dispersal – a surprising result that holds for haploidy, diploidy, and haplodiploidy (arrhenotoky). Here we develop a kin-selection model to investigate how population viscosity affects the potential for altruism in species with male paternal genome elimination (PGE), exploring altruism enacted by both females and males, and both juveniles and adults. We find that: 1) PGE promotes altruistic behaviours relative to the other inheritance systems, and to a degree that depends on the extent of paternal genome expression. 2) Under PGE, dispersal increases the potential for altruism in juveniles and decreases it in adults. 3) The genetics of PGE can lead to striking differences in sex-specific potentials for altruism, even in the absence of any sex-differences in ecology.

Scots translation (by Ashley Douglas):

Paternal genome drap-oot forders altruism in stieve populations

Population stieveness has lang been thocht tae forder the evolution o altruism. Hooivver, in the maist straucht-forrit o scenarios, the potential fur altruism is invariant wi respeck tae skail – a stamagasterin ootcome that hauds fur haploidy, diploidy, and haplodiploidy (arrhenotoky). Here we pit forrit a kin-walin model fur tae airt-oot hoo population stieveness affects the potential fur altruism in species wi male paternal genome drap-oot (PGD), takkin tent o altruism enactit by baith females and males, forby baith young-anes and aulder-anes. We find that: 1) PGD forders altruistic ongauns relative tae the ither inheritance seestems, forby tae a degree that depends on the extent o paternal genome kythin. 2) Unner PGD, skail maks mair muckle the potential fur altruism amang young-anes and gars it less likely amang aulder-anes. 3) The genetics o PGD can lead tae kenspeckle differences in sex-specific potentials fur altruism, even wioot onie sex-differences in ecology.

[New Paper] The evolution of religiosity by kin selection

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Stucky K & Gardner A (2022) The evolution of religiosity by kin selection. Religion, Brain & Behavior

Despite religion’s apparent ubiquity, hypotheses about the selection pressures that may have shaped its cognitive foundations remain controversial. Here, we develop and analyze a mathematical model inspired by Crespi and Summers’ suggestion that parent-offspring conflict has driven the evolution of religious beliefs to explore the causes and consequences of these selection pressures. To this end, we employ kin selection methodology to investigate how selection may mold an individual’s propensity for religiosity and corresponding patterns of gene expression, revealing that the evolution of religiosity is modulated by genetic relatedness between social partners, that selection in relation to religiosity may depend on an individual’s age and sex, and that religiosity can foment intragenomic conflicts of interest that give rise to parent-of-origin specific patterns of gene expression and concomitant clinical disorders. More generally, we develop a formal, theoretical framework that enables the derivation of clear-cut, comparative predictions about adaptive as well as maladaptive religiosity phenotypes.

[New Paper] Population viscosity promotes altruism under density-dependent dispersal

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Kanwal JK & Gardner A (2022) Population viscosity promotes altruism under density-dependent dispersal Proceedings of the Royal Society of London Series B – Biological Sciences289, 20212668.

A basic mechanism of kin selection is population viscosity, whereby individuals do not move far from their place of birth and hence tend to be surrounded by relatives. In such circumstances, even indiscriminate altruism among neighbours will often involve interactions between kin, which has a promoting effect on the evolution of altruism. This has the potential to explain altruistic behaviour across the whole tree of life, including in taxa for which recognition of kin is implausible. However, population viscosity may also intensify resource competition among kin, which has an inhibitory effect on altruism. Indeed, in the simplest scenario, in which individuals disperse with a fixed probability, these two effects have been shown to exactly cancel such that there is no net impact of viscosity on altruism. Here, we show that if individuals are able to disperse conditionally upon local density, they are favoured to do so, with more altruistic neighbourhoods exhibiting a higher rate of dispersal and concomitant relaxation of kin competition. Comparing across different populations or species, this leads to a negative correlation between overall levels of dispersal and altruism. We demonstrate both analytically and using individual-based simulations that population viscosity promotes the evolution of altruism under density-dependent dispersal.

[New Paper] Sex-biased demography modulates male harm across the genome

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Hitchcock TJ & Gardner A (2021) Sex-biased demography modulates male harm across the genome. Proceedings of the Royal Society of London Series B – Biological Sciences 288, 20212237.

Image created at https://app.wombo.art

Recent years have seen an explosion of theoretical and empirical interest in the role that kin selection plays in shaping patterns of sexual conflict, with a particular focus on male harming traits. However, this work has focused solely on autosomal genes, and as such it remains unclear how demography modulates the evolution of male harm loci occurring in other portions of the genome, such as sex chromosomes and cytoplasmic elements. To investigate this, we extend existing models of sexual conflict for application to these different modes of inheritance. We first analyse the general case, revealing how sex-specific relatedness, reproductive value and the intensity of local competition combine to determine the potential for male harm. We then analyse a series of demographically explicit models, to assess how dispersal, overlapping generations, reproductive skew and the mechanism of population regulation affect sexual conflict across the genome, and drive conflict between nuclear and cytoplasmic genes. We then explore the effects of sex biases in these demographic parameters, showing how they may drive further conflicts between autosomes and sex chromosomes. Finally, we outline how different crossing schemes may be used to identify signatures of these intragenomic conflicts.

[New Paper] Reproductive value and the evolution of altruism

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Rodrigues AMM & Gardner A (in press) Reproductive value and the evolution of altruism. Trends in Ecology and Evolution doi: https://doi.org/10.1016/j.tree.2021.11.007

Altruism is favored by natural selection provided that it delivers sufficient benefits to relatives. An altruist’s valuation of her relatives depends upon the extent to which they carry copies of her genes – relatedness – and also on the extent to which they are able to transmit their own genes to future generations – reproductive value. However, although relatedness has received a great deal of attention with regard to altruism, reproductive value has been surprisingly neglected. We review how reproductive value modulates patterns of altruism in relation to individual differences in age, sex, and general condition, and discuss how social partners may manipulate each other’s reproductive value to incentivize altruism. This topic presents opportunities for tight interplay between theoretical and empirical research.

[New Paper] Sexual antagonism in haplodiploids.

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Hitchcock TJ, Gardner A & Ross L (in press) Sexual antagonism in haplodiploids. Evolution doi: https://doi.org/10.1111/evo.14398 

Females and males may face different selection pressures, such that alleles conferring a benefit in one sex may be deleterious in the other. Such sexual antagonism has received a great deal of theoretical and empirical attention, almost all of which has focused on diploids. However, a sizeable minority of animals display an alternative haplodiploid mode of inheritance, encompassing both arrhenotoky, whereby males develop from unfertilized eggs, and paternal genome elimination (PGE), whereby males receive but do not transmit a paternal genome. Alongside unusual genetics, haplodiploids often exhibit social ecologies that modulate the relative value of females and males. Here we develop a series of evolutionary-genetic models of sexual antagonism for haplodiploids, incorporating details of their molecular biology and social ecology. We find that: 1) PGE promotes female-beneficial alleles more than arrhenotoky, and to an extent determined by the timing of elimination – and degree of silencing of – the paternal genome; 2) sib-mating relatively promotes female-beneficial alleles, as do other forms of inbreeding, including limited male-dispersal, oedipal-mating, and the pseudo-hermaphroditism of Icerya purchasi; 3) resource competition between related females inhibits the invasion of female-beneficial alleles; and 4) sexual antagonism foments conflicts between parents and offspring, endosymbionts and hosts, and maternal-origin and paternal-origin genes.

(Photo: https://commons.wikimedia.org/wiki/File:Sminthurides_malmgreni_courtship_(7178213310).jpg)

[New Group Member] Bing Dong

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Bing Dong has joined us to undertake a PhD. He’ll be working on genomic imprinting. Welcome to the lab, Bing!

[PhD opportunity] Social evolution: cooperation & conflict between genes, individuals & groups

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Social evolution: cooperation and conflict between genes, individuals and groups

Natural selection explains the appearance of design in the living world. But at what level is this design expected to manifest – gene, individual or group – and what is its function? Social evolution provides a window on this problem, because it is in the context of social interaction that the interests of genes, individuals and groups come into conflict with each other.

I invite applications for a PhD studentship in my research group at the School of Biology, University of St Andrews, Scotland, to develop new theory on the topic of social evolution. The project will suit a Biology graduate with a strong interest in social evolution, but applications from graduates with other backgrounds are also encouraged, and although prior experience in mathematical modelling would be helpful this is certainly not required as the requisite training will be provided.

Current research in my lab involves development of general theory – using kin selection, multilevel selection, game theory and theoretical population genetics approaches – as well as more specific mathematical and computer simulation models that are tailored to the biology of particular organisms, from microbes to insects to humans. Much of our ongoing work is focused on intragenomic conflicts and associated clinical pathologies, plus the role of sex and gender in social evolution.

This studentship is funded by the European Research Council and the School of Biology at the University of St Andrews for a duration of 3.5 years. There are no nationality restrictions on who can apply, and the studentship will cover both Home and Overseas tuition fees, as well as providing a living allowance and covering the costs of the research. (Chinese nationals are particularly encouraged to apply, as they will also be eligible for additional funding opportunities at the University of St Andrews.)

If evolutionary biology really fascinates you, and you are a careful thinker, then you will flourish in the kind of project that I enjoy supervising. Please direct informal enquiries to Prof Andy Gardner ([email protected]).

The deadline for applications is 3 Dec 2021. Details on how to apply are given here.

[New Paper] Sex, males, and hermaphrodites in the scale insect Icerya purchasi

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Mongue AJ, Michaelides S, Coombe O, Tena A, Kim D-S, Normark B, Gardner A, Hoddle MS & Ross L (2021) Sex, males, and hermaphrodites in the scale insect Icerya purchasi. Evolution doi: https://doi.org/10.1111/evo.14233

Androdioecy (the coexistence of males and hermaphrodites) is a rare mating system for which the evolutionary dynamics are poorly understood. Here we investigate the cottony cushion scale, Icerya purchasi, one of only three reported cases of androdioecy in insects. In this species, female-like hermaphrodites have been shown to produce sperm and self-fertilize. However, males are rarely observed too. In a large genetic analysis, we show for the first time that, although self-fertilization appears to be the primary mode of reproduction, rare outbreeding events between do occur in natural populations, supporting the hypothesis that hermaphrodites mate with males and androdioecy is the mating system of I. purchasi. Thus, this globally invasive pest insect appears to have the colonization advantages of a selfing organism while also benefitting from periodic reintroduction of genetic variation through outbreeding with males.

(Photo: https://commons.wikimedia.org/wiki/Category:Icerya_purchasi#/media/File:Icerya_purchasi_1.JPG)

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