The genetic basis of behavioral divergence in three-spined stickleback (Gasterosteus aculeatus)
Behrens, Colby
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https://hdl.handle.net/2142/124548
Description
Title
The genetic basis of behavioral divergence in three-spined stickleback (Gasterosteus aculeatus)
Author(s)
Behrens, Colby
Issue Date
2024-04-22
Director of Research (if dissertation) or Advisor (if thesis)
Bell, Alison M
Doctoral Committee Chair(s)
Bell, Alison M
Committee Member(s)
Fuller, Becky C
Catchen, Julian M
Fischer, Eva K
Weir, Laura K
Department of Study
Evolution Ecology Behavior
Discipline
Biology
Degree Granting Institution
University of Illinois at Urbana-Champaign
Degree Name
Ph.D.
Degree Level
Dissertation
Keyword(s)
genomics
parental care
Abstract
Behaviors are extraordinarily diverse within and among animal taxa and can play important roles in adaptive divergence and speciation. In particular, reproductive behaviors can play a key role in adaptation and can act as important prezygotic reproductive isolating barriers. However, the selective factors that drive behavioral divergence are often unclear, especially in recently diverged species or populations. Similarly, the molecular and genetic mechanisms underlying behavioral diversity are rarely understood, and dissecting the genetic basis of behaviors can be difficult due to the complex genetic architecture underlying the traits.
Here, I addressed these questions by examining behavioral and genomic divergence between a pair of recently-diverged three-spined stickleback (Gasterosteus aculeatus) known as the “white” and “common” stickleback. Typically, male three-spined stickleback provide extensive care to their developing offspring, but the “white” population has recently evolutionarily lost paternal care and diverged from the caring “common” population. This offers a unique opportunity to examine the mechanisms of natural behavioral variation between recently-diverged populations.
First, I examined life history traits in both populations of stickleback. The evolutionary origin of parental care is often associated with shifts in a variety of life history traits, so I tested the hypothesis that the evolutionary loss of care is associated with reciprocal shifts of the same traits. I found that the female white stickleback invested significantly fewer resources in their offspring, suggesting that the loss of care is associated with predictable shifts in life history traits. Second, I examined how suites of reproductive behaviors coevolve during early divergence. After performing detailed behavioral observations, I identified significant divergence in a suite of reproductive behaviors, including nest-building, courtship, and parental care. These results suggested that coevolutionary feedback between behaviors can push reproductive strategies to rapidly diverge. Third, I explored how neurogenomic patterns shift across the reproductive cycle and how these transcriptomic states differ across the populations. Hundreds of genes were differentially expressed across reproductive stages, suggesting that commons and whites exhibit unique neurogenomic profiles throughout the reproductive cycle. Additionally, data from F1 hybrids suggested that this divergence may be driven by variation in trans, rather than cis, regulatory elements. Finally, I tested the hypothesis that a multi-gene locus, or “supergene”, facilitated rapid divergence in reproductive behaviors. I identified 10 genomic loci associated with behavioral variation. These loci were primarily non-overlapping, suggesting that distinct genetic mechanisms are responsible for the divergence in reproductive strategies between commons and whites. Together, these studies highlight the value in studying natural behavioral variation and address outstanding questions about the mechanisms associated with rapid behavioral divergence.
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