Complex evolutionary processes maintain an ancient chromosomal inversion

Abstract

Genome re-arrangements such as chromosomal inversions are often involved in adaptation. As such, they experience natural selection, which can erode genetic variation. Thus, whether and how inversions can remain polymorphic for extended periods of time remains debated. Here we combine genomics, experiments, and evolutionary modeling to elucidate the processes maintaining an inversion polymorphism associated with the use of a challenging host plant (Redwood trees) in Timema stick insects. We show that the inversion is maintained by a combination of processes, finding roles for life-history trade-offs, heterozygote advantage, local adaptation to different hosts, and gene flow. We use models to show how such multi-layered regimes of balancing selection and gene flow provide resilience to help buffer populations against the loss of genetic variation, maintaining the potential for future evolution. We further show that the inversion polymorphism has persisted for millions of years and is not a result of recent introgression. We thus find that rather than being a nuisance, the complex interplay of evolutionary processes provides a mechanism for the long-term maintenance of genetic variation.

Evolved and plastic gene expression in adaptation to a novel niche

“…Inversions segregate between apple- and hawthorn-infesting populations of another Tephritid fly, Rhagoletis pomonella (Egan et al, 2015; Feder & Nosil, 2009; Ragland et al, 2017). Large inversions also underlie both a host-associated color polymorphism (Nosil et al, 2018) and inter- and intra-specific variation in feeding on redwood trees by Timema walking sticks(Nosil et al, 2023). However, experimental evidence for how inversions alter gene expression during local adaptation and divergence is still limited (Berdan et al, 2023).…”

Two Nested Inversions in the X Chromosome Differentiate the Dominant Malaria Vectors in Europe, Anopheles atroparvus and Anopheles messeae

“…A growing body of research indicates that chromosome rearrangements are significant factors in species evolution and adaptation [42][43][44]. Data obtained from various organisms suggest that chromosomal polymorphism is a mechanism that species use to adapt rapidly to climate changes [45,46].…”

A sex-linked supergene with large effects on sperm traits has little impact on reproductive traits in female zebra finches

“…Despite this, reproductive output often varies considerably between individuals, and the genetic basis of this variation is not well understood [1][2][3]. Chromosomal inversions are widespread across taxa, and inversion polymorphisms are increasingly recognized as important in the maintenance of genetic variation [4,5]. Estrildidae finches like the zebra finch (Taeniopygia guttata) are particularly prone to inversions [6,7], making them useful for studying the relationship between inversions and the maintenance of reproductive trait variation.…”