Craniofacial shape transition across the house mouse hybrid zone: implications for the genetic architecture and evolution of between-species differences

Abstract

Craniofacial shape differences between taxa have often been linked to environmental adaptation, e.g., new food sources, or have been studied in the context of domestication. Evidence for the genetic basis of such phenotypic differences to date suggests that between-species as well as betweenpopulation variation has an oligogenic basis, i.e., few loci of large effect explain most of the variation. In mice, it has been shown that within-population craniofacial variation has a highly polygenic basis, but there are no data regarding the genetic basis of between-species differences in natural populations. Here, we address this question using a phenotypefocused approach. Using 3D geometric morphometrics, we phenotyped a panel of mice derived from a natural hybrid zone between Mus musculus domesticus and Mus mus musculus and quantify the transition of craniofacial shape along the hybridization gradient. We find a continuous shape transition along the hybridization gradient and unaltered developmental stability associated with hybridization. This suggests that the morphospace between the two subspecies is continuous despite reproductive isolation and strong barriers to gene flow. We show that quantitative changes in overall genome composition generate quantitative changes in craniofacial shape; this supports a highly polygenic basis for between-species craniofacial differences in the house mouse. We discuss our findings in the context of oligogenic versus polygenic models of the genetic architecture of morphological traits.

Using the Mus musculus hybrid zone to assess covariation and genetic architecture of limb bone lengths

“…Across the hybrids, lengths of forelimbs and hindlimbs were significantly correlated with the proportion of genomic ancestry from each subspecies (Figure ). A similar pattern was observed for the transition of skull shapes across the hybrid zone, where we have argued that this is compatible with a polygenic model (Pallares et al., ).…”

“…Grey dots include values of 25 additional animals taken from Pallares et al. () for which only partial genotype data were available; that is, these were not included in the association analyses…”

“…Following the procedure described in Pallares et al. () and based on a specific SNP data set from 37 loci, we performed regressions of forelimb and hindlimb lengths versus percentage of M. m. domesticus alleles (“PairMid” in Table S1).…”

“…Mice in the hybrid zone are naturally admixed, and linkage disequilibrium is sufficiently low to allow high‐resolution mapping, including the identification of individual candidate genes (Pallares et al., ; Turner & Harr, ). Further, the continuous transition in genomic composition from one subspecies to the other allows inferences about the genetic architecture and evolution of morphological traits (Pallares, Turner, & Tautz, ).…”

Genetic constraints on wing pattern variation in Lycaeides butterflies: A case study on mapping complex, multifaceted traits in structured populations

“…Such a polygenic architecture is unsurprising within populations and nominal taxa, but is perhaps less expected at the species‐complex level as it is not uncommon for major‐effect loci to contribute to phenotypic differences between species (Martin & Orgogozo, ; Orr, ; Stern & Orgogozo, ). Nonetheless, a polygenic basis for both between‐ and within‐species differences has been detected in other systems, such as craniofacial traits in mice (Pallares, Turner, & Tautz, ; Pallares et al., ), and might be more likely when selection plays only a minor role in trait divergence between species. We know that wing pattern is involved in species/mate recognition in Lycaeides (Fordyce et al., ; Gompert, Lucas, Nice, Fordyce, et al., ), but whether selection was responsible for the evolution of wing pattern differences (not just the maintenance of these differences) is unclear.…”