The Evolution of Nesting Behavior in Peromyscus Mice

Abstract

To understand how behavior evolves, it is necessary to understand how genetic divergence between species modifies neural circuits and, ultimately, behavior. Here I examine divergence in Peromyscus nesting behavior—the collection and processing of environmental materials to build a structure of thermoregulatory value—at multiple levels. I first characterize nesting in virgin animals from seven taxa of Peromyscus mice and find that species largely vary in their latency to build equivalently-shaped nests. I then focus on animals from the sister species Peromyscus polionotus subgriseus (the oldfield mouse), which are quick to nest, and P. maniculatus bairdii (the deer mouse), which are slow to nest. Nesting appears to be a sleep-preparatory behavior for these nocturnal species, with P. polionotus animals nesting at the onset of their light cycle. Immediate-early gene expression patterns suggest that the neural basis of this behavioral difference is complex. To investigate the genetic basis of this heritable species difference, I use the nesting behavior of 832 animals from an F2 intercross mapping population (P. maniculatus x P. polionotus) and a multiplexed shotgun genotyping strategy to identify three quantitative trait loci (QTL) associated with nesting latency. The QTL most strongly associated with nesting latency spans a region of Peromyscus chromosome 9 that contains only 54 annotated protein-coding genes, 22 of which are differentially expressed in the adult brain due to cis-regulatory divergence between the two species. While these are all plausible candidates to explain the species difference, the most striking candidates are Dach1, Pcdh17, and Pcdh20, which have significant expression differences in the medial prefrontal cortex or striatum, brain regions important for emotional decision-making and motivation. Finally, I use a comparative transcriptomic approach to explore transcriptional variation in an additional subspecies of P. maniculatus, P. maniculatus nubiterrae, which has polionotus-like nesting behavior. With the caveat that our power to detect species differences is lower in this dataset, the transcriptional mechanisms underlying these species differences may be distinct. Together, these experiments build a foundation for understanding the precise genetic mechanisms responsible for divergence in an adaptive behavior, which will have important implications for our understanding of behavioral evolution.