Sexual imprinting and speciation between two Peromyscus species

Abstract

Sexual isolation, a reproductive barrier, can prevent interbreeding between diverging populations or species. Sexual isolation can have a clear genetic basis; however, it may also result from learned mate preferences that form via sexual imprinting. Here, we demonstrate that two sympatric species of mice-the white-footed mouse (Peromyscus leucopus) and its sister species, the cotton mouse (P. gossypinus)-hybridize only rarely in the wild despite co-occurrence in the same habitat and lack of any measurable intrinsic postzygotic barriers in laboratory crosses. We present evidence that strong conspecific mating preferences in each species result in significant sexual isolation. We find that these preferences are learned in at least one species: P. gossypinus sexually imprints on its parents, but in P. leucopus, additional factors influence mating preferences. Our study demonstrates that sexual imprinting contributes to reproductive isolation that reduces hybridization between otherwise interfertile species, supporting the role for learning in mammalian speciation.

Diet‐based assortative mating through sexual imprinting

“…While dietary information was learnable and led to some assortative mating preferences in females, male preferences appeared random with respect to diet. Although a number of other studies have found sex‐specific differences in the degree or strength of sexual imprinting (e.g., Delaney & Hoekstra, ; Kozak, Head, & Boughman, ; Verzijden et al, ; Verzijden, Korthof, & Cate, ; Witte & Sawka, ), the sex difference observed here was surprising as we previously established that both P. gossypinus males and females strongly sexually imprint on their parents in a cross‐fostering experiment with P. leucopus (Delaney & Hoekstra, ). Thus, males are capable of sexual imprinting but in this study either failed to imprint on diet, imprinted on diet but relied more heavily on other cues (e.g., visual, vocal, or chemical cues; Rosenthal, ) to select mates, or we were unable to detect this pattern due to limited sample sizes.…”

“…To assess whether male and female choosers preferred stimuli based on their parental diet, we recorded each chooser's most preferred stimulus (defined as whichever stimulus the chooser spent more time with). We previously showed that the proportion of time a chooser spent with a stimulus in our gated mate choice apparatus near‐perfectly predicts copulation (Delaney & Hoekstra, ), allowing us to convert chooser preference to a binary variable (garlic mate preferred or orange mate preferred). Then, we used one‐sided Fisher's Exact tests to determine if preferences for garlic versus orange were significantly different between females by diet and/or between males by diet.…”

“…We established our laboratory population of Peromyscus gossypinus from wild‐caught individuals in 2009 (see Delaney & Hoekstra, ). We maintained a large colony of mice on a standard diet (Purina Iso Pro 5P76) and manipulated diets by adding novel, artificial flavors to their water.…”

“…Using an electronically controlled gated choice apparatus (Figure a; described in Delaney & Hoekstra, ), we tested the mating preferences of adult mice (>80 days old) for opposite sex stimulus individuals that were raised on either garlic‐ or orange‐flavored water. In brief, we implanted all mice with small radio‐frequency identification (RFID) transponders (1.4 mm × 9 mm, ISO FDX‐B, Planet ID Gmbh) in the interscapular region.…”

“…Here, we experimentally test the hypothesis that divergence in diet, when sexually imprinted, can lead to assortative mating. Specifically, we manipulated diet in P. gossypinus , a rodent species that can form mating preferences through sexual imprinting strong enough to establish a sexual reproductive isolating barrier from its sister species, P. leucopus (Delaney & Hoekstra, ). Thus, diet could enhance the degree of sexual isolation between this species pair, which is known to consume different foods in sympatry (Calhoun, ).…”