Temperature-dependent gene regulatory divergence underlies local adaptation with gene flow in the Atlantic silverside

Arne Jacobs; Jonathan P Velotta; Anna Tigano; Aryn P Wilder; Hannes Baumann; Nina O Therkildsen

doi:10.1093/evolut/qpae049

Temperature-dependent gene regulatory divergence underlies local adaptation with gene flow in the Atlantic silverside

Evolution. 2024 Mar 22:qpae049. doi: 10.1093/evolut/qpae049. Online ahead of print.

Authors

Arne Jacobs^{1

2}, Jonathan P Velotta^{1

3}, Anna Tigano^{1

4}, Aryn P Wilder^{1

5}, Hannes Baumann⁶, Nina O Therkildsen¹

Affiliations

¹ Department of Natural Resources and the Environment, Cornell University, Ithaca, New York, USA.
² School of Biodiversity, One Health and Veterinary Medicine, University of Glasgow, Glasgow, UK.
³ Department of Biological Sciences, University of Denver, Denver, Colorado, USA.
⁴ Department of Biology, The University of British Columbia, Okanagan Campus, Kelowna, British Columbia, Canada.
⁵ San Diego Zoo Wildlife Alliance, Escondido, California, USA.
⁶ Department of Marine Sciences, University of Connecticut, Groton, Connecticut, USA.

PMID: 38517121
DOI: 10.1093/evolut/qpae049

Abstract

Gene regulatory divergence is thought to play an important role in adaptation, yet its extent and underlying mechanisms remain largely elusive for local adaptation with gene flow. Local adaptation is widespread in marine species despite generally high connectivity and is often associated with tightly linked genomic architectures, such as chromosomal inversions. To investigate gene regulatory evolution under gene flow and the role of inversions associated with local adaptation to a steep thermal gradient, we generated RNA-seq data from Atlantic silversides (Menidia menidia) from two locally adapted populations and their F1 hybrids, reared under two temperatures. We found substantial divergence in gene expression and thermal plasticity between populations, with up to 31% of genes being differentially expressed. Reduced thermal plasticity, temperature-dependent gene misexpression and the disruption of co-expression networks in hybrids point towards a role of regulatory incompatibilities in local adaptation, particularly under colder temperatures. Chromosomal inversions show an accumulation of regulatory incompatibilities but are not consistently enriched for differentially expressed genes. Together, these results suggest that gene regulation can diverge substantially among populations despite gene flow, partly due to the accumulation of temperature-dependent regulatory incompatibilities within inversions.

Keywords: Gene expression; Gene flow; Gene regulatory incompatibilities; Hybrid gene misexpression; Local adaptation; Marine fish; Regulatory architecture.