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Giant island mice exhibit widespread gene regulatory evolution in key metabolic organs

ABSTRACT: Background: Island populations repeatedly evolve extreme body sizes, but the genomic basis of this morphological pattern remains largely unknown. To understand how organisms on islands evolve gigantism, we compared genome-wide patterns of gene expression in Gough Island mice, the largest wild house mice in the world, and mice from the WSB/EiJ wild-derived inbred strain. In a highly replicated experiment, we used RNASeq to quantify differences in gene expression in three key metabolic organs: gonadal adipose depot, hypothalamus, and liver. Results: We discovered pervasive evidence of transcriptional evolution, with 20% or more of differentially regulated transcripts in each organ exhibiting expression fold changes of at least 2X. By considering differential expression jointly with the genomic positions of quantitative trait loci for body size and single nucleotide differences located within established tissue-specific regulatory elements, we nominated 66 candidate genes for extreme size evolution, including Irs1 and Lrp1. Patterns of differential expression across three developmental time points in the liver revealed that Arid5b potentially regulates tens of co-regulated gene groups. Functional enrichment analyses on thousands of differentially expressed genes pointed to cell cycling, mitochondrial function, signaling pathways, immune reactivity, and nutrient metabolism as potential causes of weight accumulation in Gough Island mice. Conclusion: Collectively, our results suggest that extensive regulatory evolution in metabolic organs contributed to the rapid evolution of gigantism during the short time house mice have inhabited Gough Island.

ORGANISM(S): Mus musculus domesticus

PROVIDER: GSE135007 | GEO | 2020/09/18

REPOSITORIES: GEO

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Project description:Background Appropriate social interactions influence animal fitness by impacting several processes, such as mating, territory defense, and offspring care. Many studies shedding light on the neurobiological underpinnings of social behavior have focused on nonapeptides (vasopressin, oxytocin, and homologues) and on sexual or parent-offspring interactions. Furthermore, animals have been studied under artificial laboratory conditions, where the consequences of behavioral responses may not be as critical as when expressed under natural environments, therefore obscuring certain physiological responses. We used automated recording of social interactions of wild house mice outside of the breeding season to detect individuals at both tails of a distribution of egocentric network sizes (characterized by number of different partners encountered per day). We then used RNA-seq to perform an unbiased assessment of neural differences in gene expression in the prefrontal cortex, the hippocampus and the hypothalamus between these mice with naturally occurring extreme differences in social network size. Results We found that the neurogenomic pathways associated with having extreme social network sizes differed between the sexes. In females, hundreds of genes were differentially expressed between animals with small and large social network sizes, whereas in males very few were. In males, X-chromosome inactivation pathways in the prefrontal cortex were the ones that better differentiated animals with small from those with large social network sizes animals. In females, animals with small network size showed up-regulation of dopaminergic production and transport pathways in the hypothalamus. Additionally, in females, extracellular matrix deposition on hippocampal neurons was higher in individuals with small relative to large social network size. Conclusions Studying neural substrates of natural variation in social behavior in traditional model organisms in their habitat can open new targets of research for understanding variation in social behavior in other taxa.

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Giant island mice exhibit widespread gene regulatory evolution in key metabolic organs

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