Trade-offs beget trade-offs: Causal analysis of mammalian population dynamics

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Abstract

Survival and reproduction strategies in mammals are determined by trade-offs between life history traits. In turn, the unique configuration of traits that characterizes mammalian species gives rise to species-specific population dynamics. The dependence of population dynamics on life history has been primarily studied as the relationship between population density and size-related traits. With the recent accumulation of genomic data, the effective population size (number of breeding individuals; N e ) over the last 100-800 kya has become quantifiable for a large proportion of mammals. Using phylogenetic path analysis, we compared the dependence of population density and N e on eleven traits that characterize mammalian allometry, diet and reproduction. We found variable trait impacts on these two metrics of population dynamics across different phylogenetic, ecological and conservation classifications of mammals. Brain size had a negative effect on density but a positive effect on N e , especially in primates and carnivores. Diet specialization had a negative effect on both density and N e . The relationship between N e (but not density) and several traits showed biome-related gradients. We found that critically endangered species have life history strategies that impede population recovery, as reflected by the strong positive dependence of both density and N e on generation length. Our findings demonstrate that trade-offs characterizing life history evolution are not only trait-specific, but are also present between different metrics of population dynamics. This challenges the static nature of the “energetic equivalence” rule and has major implications for selecting the appropriate population metric in species conservation and restoration strategies.

Significance statement

Trade-offs are an essential component of trait evolution, underlying various strategies used by species to mitigate environmental pressures and ensure their survival. We investigated how traits affect mammalian population-level parameters, including population density and effective population size (number of breeding individuals; N e ). We found that the impact of traits on these two measures of population dynamics was variable. For example, both density and N e decreased in species with larger body size, while brain size was negatively related to population density but positively related to N e . We therefore show that evolutionary trade-offs are not limited to traits, but are also present between population-level parameters, which can have important implications for future conservation and restoration efforts.

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