Diet-based assortative mating through sexual imprinting

Abstract

Speciation is facilitated by "magic traits," where divergent natural selection on such traits also results in assortative mating. In animal populations, diet has the potential to act as a magic trait if populations diverge in consumed food that incidentally affects mating and therefore sexual isolation. While diet-based assortative mating has been observed in the laboratory and in natural populations, the mechanisms causing positive diet-based assortment remain largely unknown. Here, we experimentally created divergent diets in a sexually imprinting species of mouse, Peromyscus gossypinus (the cotton mouse), to test the hypothesis that sexual imprinting on diet could be a mechanism that generates rapid and significant sexual isolation. We provided breeding pairs with novel garlic- or orange-flavored water and assessed whether their offspring, exposed to these flavors in utero and in the nest before weaning, later preferred mates that consumed the same flavored water as their parents. While males showed no preference, females preferred males of their parental diet, which is predicted to yield moderate sexual isolation. Thus, our experiment demonstrates the potential for sexual imprinting on dietary cues learned in utero and/or postnatally to facilitate reproductive isolation and potentially speciation.

Open research badges: This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.n1qq6v3.

Keywords: Peromyscus; deer mouse; learning; mate choice; reproductive isolation; sexual isolation; speciation.

Figure 1

Diet‐based assortative mating preferences in Peromyscus gossypinus. (a) Schematic of the electronically controlled gated mate choice apparatus used to measure mating preferences. The apparatus contains three rat cages, each separated by RFID‐activated antennae and gates. In the scenario depicted, an orange “chooser” mouse is given a choice between two “stimuli” mice (fed either garlic or orange) of the opposite sex. (b) Proportion of time the chooser mouse spent with the two stimuli mice. The dotted line represents equal time with both stimuli: values above the line indicated the garlic stimulus was preferred, and below, the orange stimulus was preferred. Each dot represents the preference of a chooser mouse that was raised with either garlic‐fed (blue) or orange‐fed (orange) parents. Solid bars depict the median preference per group. Sample sizes are indicated in parentheses under each treatment type