4.7 Article

Complementary genomic and epigenomic adaptation to environmental heterogeneity

Journal

MOLECULAR ECOLOGY
Volume 31, Issue 13, Pages 3598-3612

Publisher

WILEY
DOI: 10.1111/mec.16500

Keywords

adaptive evolution; biological invasion; epigenetic adaptation; genetic adaptation; natural selection

Funding

  1. National Natural Science Foundation of China [42106098, 32061143012, 31772449, 32170417]
  2. Youth Innovation Promotion Association of the Chinese Academy of Sciences [2018054]
  3. Thousand PhD Program of Guangdong Academy of Sciences [2020GDASYL-20200103099]
  4. Shanghai Sailing Programme [21YF1403200]
  5. Guangdong Basic and Applied Basic Research Foundation [2019A1515110455]
  6. NSERC
  7. Canada Research Chair in Aquatic Invasive Species

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Recent studies have shown that adaptation is not only due to selection on DNA sequence-based variation, but also influenced by epigenetic factors. This study examined the genetic and epigenetic mechanisms underlying environmental adaptation in a marine invasive tunicate species. The results revealed clear population differentiation at both the genetic and epigenetic levels, with local environmental variables playing a significant role. Minimum annual sea surface temperature was identified as the top explanatory variable for both genetic and epigenetic variation. The patterns of population structure driven by genetic and epigenetic variation were somewhat distinct, suggesting some autonomy of epigenetic variation. Shared and specific genes and biological pathways associated with environmental factors were identified, indicating complementary and independent contributions of genetic and epigenetic variation to environmental adaptation in this system. These mechanisms may facilitate population persistence under environmental change and successful invasions across novel environments.
While adaptation is commonly thought to result from selection on DNA sequence-based variation, recent studies have highlighted an analogous epigenetic component as well. However, the relative roles of these mechanisms in facilitating population persistence under environmental heterogeneity remain unclear. To address the underlying genetic and epigenetic mechanisms and their relationship during environmental adaptation, we screened the genomes and epigenomes of nine global populations of a predominately sessile marine invasive tunicate, Botryllus schlosseri. We detected clear population differentiation at the genetic and epigenetic levels. Patterns of genetic and epigenetic structure were significantly influenced by local environmental variables. Among these variables, minimum annual sea surface temperature was identified as the top explanatory variable for both genetic and epigenetic variation. However, patterns of population structure driven by genetic and epigenetic variation were somewhat distinct, suggesting possible autonomy of epigenetic variation. We found both shared and specific genes and biological pathways among genetic and epigenetic loci associated with environmental factors, consistent with complementary and independent contributions of genetic and epigenetic variation to environmental adaptation in this system. Collectively, these mechanisms may facilitate population persistence under environmental change and sustain successful invasions across novel environments.

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