Evolution and Genetics of Precocious Burrowing Behavior in Peromyscus Mice

Abstract

A central challenge in biology is to understand how innate behaviors evolve between closely related species. One way to elucidate how differences arise is to compare the development of behavior in species with distinct adult traits [1]. Here, we report that Peromyscus polionotus is strikingly precocious with regard to burrowing behavior, but not other behaviors, compared to its sister species P. maniculatus. In P. polionotus, burrows were excavated as early as 17 days of age, whereas P. maniculatus did not build burrows until 10 days later. Moreover, the well-known differences in burrow architecture between adults of these species-P. polionotus adults excavate long burrows with an escape tunnel, whereas P. maniculatus dig short, single-tunnel burrows [2-4]-were intact in juvenile burrowers. To test whether this juvenile behavior is influenced by early-life environment, we reciprocally cross-fostered pups of both species. Fostering did not alter the characteristic burrowing behavior of either species, suggesting that these differences are genetic. In backcross hybrids, we show that precocious burrowing and adult tunnel length are genetically correlated and that a P. polionotus allele linked to tunnel length variation in adults is also associated with precocious onset of burrowing in juveniles, suggesting that the same genetic region-either a single gene with pleiotropic effects or linked genes-influences distinct aspects of the same behavior at these two life stages. These results raise the possibility that genetic variants affect behavioral drive (i.e., motivation) to burrow and thereby affect both the developmental timing and adult expression of burrowing behavior.

Indirect effects on fitness between individuals that have never met via an extended phenotype

“…; Metz et al . ), building nests (Perna & Theraulaz ) or caching resources within them (Larivée et al . ).…”

“…Extended phenotypes have received much theoretical interest since Dawkins (Dawkins 1978(Dawkins , 2004Jones et al 1994Jones et al , 1997Sterelny et al 1996;Jablonka 2004;Turner 2004;Hunter 2009;Bailey 2012), but extending empirical work to a range of systems has lagged behind. Individuals of many species hold territories that they may modify, for instance by digging out burrows (Weber et al 2013;Metz et al 2017), building nests (Perna & Theraulaz 2017) or caching resources within them (Lariv ee et al 2010). Additionally, organisms may alter the environment by constructing some structure in it, such as a spider's web (Blamires et al 2017a,b), or leave scent cues to be detected by others (Cisterne et al 2014).…”

BRICseq bridges brain-wide interregional connectivity to neural activity and gene expression in single animals

“…Reducing the number of subjects also leads to a substantial decrease in the total cost, both in terms of money and labor. The reduction in the number of subjects is particularly appealing for the study of non-human primates (Izpisua Belmonte et al, 2015), as well as of relatively new model systems for which connectivity maps are not yet available or individual subjects are particularly valuable, such as the Alston's singing mouse Okobi et al, 2019) and peromyscus (Bedford and Hoekstra, 2015;Metz et al, 2017;Weber et al, 2013).…”

Evolutionary diversity as a catalyst for biological discovery

“…are genetic mosaics of the parent species, and can be used for quantitative trait loci (QTL) mapping of genes contributing to species-specific behaviors. QTL mapping has been used to identify genetic loci associated with many traits of interest in Malawi cichlids (Holzman & Hulsey, 2017; Husemann et al, 2017; Nandamuri et al, 2017; O’Quin et al, 2012; Parnell et al, 2008; 2012; Parsons et al, 2015; Selz et al, 2014; Svensson et al, 2011); and has recently been used to discover genetic loci contributing to extended phenotypes (burrow structures) and social behaviors in Peromyscus mice (Bendesky et al, 2017; Metz et al, 2017; Weber et al, 2013). …”