bioRxiv Science⌕ Search

Biology subjects

Mullon, C. D. L.

Publications and source records attributed to Mullon, C. D. L..

7 recordsLinked to original sources

The moulding of intra-specific diversity by selection under ecological inheritance

Organisms continuously modify their environment, often impacting the fitness of future conspecifics due to ecological inheritance. When this inheritance is biased towards kin, selection favours modifications that increase the fitness of downstream individuals. How such selection shapes trait variation within populations remains poorly understood. Using mathematical modelling, we investigate the coevolution of multiple traits in a group-structured population when these traits affect the group environment, which is then bequeathed to future generations. We examine when such coevolution favours polymorphism as well as the resulting associations among traits. We find in particular that two traits become associated when one trait affects the environment while the other influences the likelihood that future kin experience this environment. To illustrate this, we model the coevolution of (a) the attack rate on a local renewable resource, which deteriorates environmental conditions, with (b) dispersal between groups, which reduces the likelihood that kin suffers from such deterioration. We show this often leads to the emergence of two highly-differentiated morphs: one that readily disperses and depletes local resources; and another that maintains these resources and tends to remain philopatric. More broadly, we suggest that ecological inheritance can contribute to phenotypic diversity and lead to complex polymorphism.

evolutionary biology↗

Foraging for locally and spatially varying resources: Where exploitation competition, local adaptation and kin selection meet

In patch- or habitat-structured populations different processes can lead to diversity at different scales. While spatial heterogeneity generates spatially disruptive selection favoring variation between patches, local competition can lead to locally disruptive selection promoting variation within patches. So far, almost all theory has studied these two processes in isolation. Here, we use mathematical modelling to investigate how resource variation within and between habitats influences the evolution of variation in a consumer population where individuals compete in finite patches connected by dispersal. We find that locally and spatially disruptive selection typically act in concert, favoring polymorphism under a significantly wider range of conditions than when in isolation. But when patches are small and dispersal between them is low, kin competition inhibits the emergence of polymorphism, especially when driven by local competition. We further use our model to clarify what comparisons between trait and neutral genetic differentiation (Qst/Fst comparisons) can tell about the nature of selection. Overall, our results help understand the interaction between two major drivers of diversity: locally and spatially disruptive selection; and how this interaction is modulated by the unavoidable effects of kin selection under limited dispersal.

evolutionary biology↗

Evolution of warfare by resource raiding favors polymorphism in belligerence and bravery

From protists to primates, intergroup aggression and warfare over resources has been observed in several taxa whose populations typically consist of groups connected by limited genetic mixing. Here, we model the co-evolution between four traits relevant to this setting: (i) investment into common-pool resource production within groups ("helping"); (ii) proclivity to raid other groups to appropriate their resources ("bel-ligerence"); and investments into (iii) defense and (iv) offense of group contests ("defensive and offensive bravery"). We show that when traits co-evolve, the population often experiences disruptive selection favouring two morphs: "Hawks", who express high levels of both belligerence and offensive bravery; and "Doves", who express neither. This social polymorphism involves further among-traits associations when the fitness costs of helping and bravery interact. In particular if helping is antagonistic with both forms of bravery, co-evolution leads to the coexistence of individuals that either: (i) do not participate into common-pool resource production but only in its defense and appropriation ("Scrounger Hawks"); or (ii) only invest into common pool resource production ("Producer Doves"). Provided groups are not randomly mixed, these findings are robust to several modelling assumptions. This suggests that inter-group aggression is a potent mechanism in favoring within-group social diversity and behavioural syndromes.

evolutionary biology↗

Hybridization enables the fixation of selfish queen genotypes in eusocial colonies

A eusocial colony typically consists of two main castes: queens that reproduce and sterile workers that help them. This division of labour however is vulnerable to genetic elements that favour the development of their carriers into queens. Several factors, such as intra-colonial relatedness, can modulate the spread of such caste-biasing genotypes. Here we investigate the effects of a notable yet understudied ecological setting: where larvae produced by hybridization develop into sterile workers. Using mathematical modelling, we show that the coevolution of hybridization with caste determination readily triggers an evolutionary arms race between non-hybrid larvae that increasingly develop into queens, and queens that increasingly hybridize to produce workers. Even where hybridization reduces worker function and colony fitness, this race can lead to the loss of developmental plasticity and to genetically hard-wired caste determination. Overall, our results may help understand the repeated evolution towards remarkable reproductive systems (e.g. social hybridogenesis) observed in many ant species.

evolutionary biology↗

Sex allocation, inbreeding, and measures of population differentiation in hermaphroditic metapopulations

Selection in inbred populations is expected to favor female-biased sex ratios in dioecious populations as a result of local mate competition, a prediction that finds strong support in situations where females have control of the sex ratio. Local mate competition due to inbreeding should also promote female-biased sex allocation in hermaphrodites, with reduced emphasis on the production and dispersal of sperm or pollen relative to that of eggs, ovules or seeds. While inbreeding can be the direct result of the mating system in local populations, it can also be brought about by population turnover in metapopulations with frequent local extinction and recolonization. This effect of population turnover has previously been considered for species with separate sexes. Here, we use both formal analysis and individual-based simulations to explore the effect of population turnover on sex allocation in partially self-fertilizing hermaphroditic metapopulations. Using simulations, we also assess the extent to which different genetic measures of inbreeding and population differentiation predict the equilibrium sex allocation. We find that population turnover can select for strongly female-biased sex allocation in hermaphroditic metapopulations, particularly if amongdeme dispersal is low, even where local demes are fully outcrossing. In such situations, FST is a good predictor of the equilibrium sex allocation, and much better than the alternative differentiation measures GST and Josts D. Our study extends predictions for sex allocation in subdivided populations to hermaphroditic species, and draws attention in general to the power of Wrights hierarchical inbreeding statistics to predict the sex allocation in metapopulations at equilibrium.

evolutionary biology↗

Dispersal alters the nature and scope of sexually antagonistic variation

Intralocus sexual conflict, or sexual antagonism, occurs when alleles have opposing fitness effects in the two sexes. Previous theory suggests that sexual antagonism is a driver of genetic variation by generating balancing selection. However, most of these studies assume that populations are well-mixed, neglecting the effects of spatial subdivision. Here we use mathematical modelling to show that limited dispersal changes evolution at sexually antagonistic autosomal and X-linked loci due to inbreeding and sex-specific kin competition. We find that if the sexes disperse at different rates, kin competition within the philopatric sex biases intralocus conflict in favour of the more dispersive sex. Furthermore, kin competition diminishes the strength of balancing selection relative to genetic drift, reducing genetic variation in small subdivided populations. Meanwhile, by decreasing heterozygosity, inbreeding reduces the scope for sexually antagonistic polymorphism due to nonadditive allelic effects, and this occurs to a greater extent on the X-chromosome than autosomes. Overall, our results indicate that spatial structure is a relevant factor in predicting where sexually antagonistic alleles might be observed. We suggest that sex-specific dispersal ecology and demography can contribute to interspecific and intragenomic variation in sexual antagonism.

evolutionary biology↗

Evolutionary feedbacks between genes and their extended effects under limited gene flow and biased ecological inheritance

Organisms continuously modify their living conditions via extended genetic effects on their envi-ronment, microbiome, and in some species culture. These effects can impact the fitness of current but also future conspecifics due to non-genetic transmission via ecological or cultural inheritance. In this case, selection on a gene with extended effects depends on the degree to which current and future genetic relatives are exposed to modified conditions. Here, we detail the selection gradient on a quantitative trait with extended effects in a patch-structured population, when gene flow between patches is limited and ecological inheritance within patches can be biased towards offspring. Such a situation is relevant to understand evolutionary driven changes in individual condition that can be preferentially transmitted from parent to offspring, such as cellular state, micro-environments (e.g., nests), pathogens, microbiome, or culture. Our analysis quantifies how the interaction between limited gene flow and biased ecological inheritance influences the joint evolutionary dynamics of traits together with the conditions they modify, helping understand adaptation via non-genetic modifications. As an illustration, we apply our analysis to a gene-culture coevolution scenario in which genetically-determined learning strategies coevolve with adaptive knowledge. In particular, we show that when social learning is synergistic, selection can favour strategies that generate remarkable levels of knowledge under intermediate levels of both vertical cultural transmission and limited dispersal. More broadly, our theory yields insights into the interplay between genetic and non-genetic inheritance, with implications for how organisms evolve to transform their environments.

evolutionary biology↗