American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Demography-dispersal trait correlations modify the eco-evolutionary dynamics of range expansion”

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Brad M. Ochocki, Julia B. Saltz, and Tom E. X. Miller (Feb 2020)

Read the Article (Just Accepted)

Genetic correlations constrain rapid evolution during range expansion

A <i>Callosobruchus maculatus</i> beetle. <br />(Credit: Jeff Fitlow/Rice University)
A Callosobruchus maculatus beetle.
(Credit: Jeff Fitlow/Rice University)

Many species are expanding their ranges into novel territory. Understanding and predicting the speed of range expansion are long-standing goals with important practical applications for the spread of introduced species and migration by native species in response to climate change. Genetic variation in movement and reproductive potential – the traits thought to control the rate of expansion – sets the stage for rapid evolution, which can affect expansion speed. But what happens when there genetic covariation between these traits?

Brad Ochocki and colleagues measured the genetic covariance between dispersal and reproduction in the seed beetle Callosobruchus maculatus, a laboratory model organism for the study of spatial population dynamics. They found that beetles that dispersed very far had reduced reproductive output, and vice versa. This genetic correlation acted as an evolutionary constraint, dampening the extent to which rapid evolution can accelerate range expansion. The authors then used mathematical models to generalize beyond the beetle system to show that, under some conditions, genetically based trade-offs can even cause an evolutionary slowdown of range expansion, since strong dispersers at the leading range edge have poor reproductive performance. The results suggest that rapid evolution should be incorporated into forecasts for range expansion, but that genetic correlations between key expansion traits can generate more diverse eco-evolutionary outcomes than expected under classic models with independently evolving traits.


Abstract

Spreading populations are subject to evolutionary processes acting on dispersal and reproduction that can increase invasion speed and variability. It is typically assumed that dispersal and demography traits evolve independently, but abundant evidence points to correlations between them that may be positive or negative and genetic, maternal, or environmental. We sought to understand how demography-dispersal correlations modify the eco-evolutionary dynamics of range expansion. We first explored this question with the beetle Callosobruchus maculatus, a laboratory model in which evolutionary acceleration of invasion has been demonstrated. We then built a simulation model to explore the role of trait correlations in this system and more generally. We found that positive correlations amplify the positive influence of evolution on speed and variability, while negative correlations (such as we found empirically) constrain that influence. Strong negative genetic correlations can even cause evolution to decelerate invasion. Genetic and non-genetic (maternal and environmental) correlations had similar effects on some measures of invasion but different effects on others. Model results enabled us to retrospectively explain invasion dynamics and trait evolution in C. maculatus, and may similarly aid the interpretation of other field and laboratory studies. Non-independence of demography and dispersal is an important consideration for understanding and predicting outcomes of range expansion.