Dynamics of genomic change during evolutionary rescue in the seed beetle Callosobruchus maculatus

Abstract

Rapid adaptation can prevent extinction when populations are exposed to extremely marginal or stressful environments. Factors that affect the likelihood of evolutionary rescue from extinction have been identified, but much less is known about the evolutionary dynamics (e.g., rates and patterns of allele frequency change) and genomic basis of successful rescue, particularly in multicellular organisms. We conducted an evolve‐and‐resequence experiment to investigate the dynamics of evolutionary rescue at the genetic level in the cowpea seed beetle, Callosobruchus maculatus, when it is experimentally shifted to a stressful host plant, lentil. Low survival (~1%) at the onset of the experiment caused population decline. But adaptive evolution quickly rescued the population, with survival rates climbing to 69% by the F5 generation and 90% by the F10 generation. Population genomic data showed that rescue likely was caused by rapid evolutionary change at multiple loci, with many alleles fixing or nearly fixing within five generations of selection on lentil. Selection on these loci was only moderately consistent in time, but parallel evolutionary changes were evident in sublines formed after the lentil line had passed through a bottleneck. By comparing estimates of selection and genomic change on lentil across five independent C. maculatus lines (the new lentil‐adapted line, three long‐established lines and one case of failed evolutionary rescue), we found that adaptation on lentil occurred via somewhat idiosyncratic evolutionary changes. Overall, our results suggest that evolutionary rescue in this system can be caused by very strong selection on multiple loci driving rapid and pronounced genomic change.

Genetic signatures of evolutionary rescue by a selective sweep

“…It is, of course, difficult to say in any case -without observing replicate populations go extinct or performing experiments -whether extinction would have occurred (or will occur) without adaptive evolution, as required by the strict definition of evolutionary rescue. We therefore need more experiments (such as Rêgo et al, 2019) that explore the genetic consequences of verified rescue to confirm the theoretical results presented here and help develop a robust signal of rescue to compare patterns from natural populations to. A strength of the above analysis is that we have explicitly modelled a feedback between demography and evolution, restricting the range of genetic signatures we consequently expect to observe.…”

High standing genetic variation in an invasive plant allows immediate evolutionary response to climate warming

“…One component for such evolutionary changes in invasive species can be the increased genetic variation and of novel or transgressive phenotypes created through admixtures 11,12,25 . In addition, a small number of loci with large phenotypic effects 55 , or strong directional selection 56 as in our study, may further contribute to rapid evolution. Here, we found significant genetic divergence in several phenotypic traits of ragweed populations under warming selection.…”

Combining Experimental Evolution and Genomics to Understand How Seed Beetles Adapt to a Marginal Host Plant

“…Population-genomic approaches include genome scans for detecting selection and the use of evolve-and-resequence (E&R) experiments (e.g., [34][35][36]). These approaches are similar in that they examine the outcomes of evolution and thus inherently integrate across the various sources and targets of selection [37,38]. Experimental evolution studies typically include replication, precise control of environmental conditions, known demographic conditions, and temporal sampling, all of which aid in identifying genes responsible for adaptation (e.g., [33,37,[39][40][41]).…”

“…It has long served as a model system for investigating the evolution of insect-plant interactions [58][59][60], and has been used more recently to examine a variety of questions in evolutionary biology, especially those involving sexual selection and sexual conflict (e.g., [61][62][63][64][65]). Because of current advances in genomic resources, this system is poised as an emerging model system for evolutionary genomics as well [38,66,67].…”

“…Beetle populations mainly attack grain legumes in the tribe Phaseoleae, particularly those in the genus Vigna [69]. Lentil (Lens culinaris), a member of the tribe Fabeae, is a very poor host for most C. maculatus populations, as larval survival in seeds is typically <5% [38,[70][71][72]. Nonetheless, lentil is used as a host by a few unusual ecotypes in certain regions [73,74].…”