Hybridization may promote variation in cognitive phenotypes in experimental guppy hybrids

Abstract

Hybridization is an underappreciated mechanism of evolution. While hybrids often express inferior traits and are selected against, hybridization can promote phenotypic variation and produce trait combinations distinct from the parentals, generating novel adaptive potential. Among other traits, hybridization can impact behaviour and cognition and may reinforce species boundaries when hybrids show decreased cognitive abilities. However, the hypothesized role of hybridization in the diversification of cognitive phenotypes remains enigmatic. To test this idea, we compare the performance of guppies (Poecilia reticulata), Endler’s guppies (Poecilia wingei), and their experimental hybrids in colour association and reversal learning. In addition, we introduce a new approach to compare multidimensional cognitive phenotypes. We found that hybrids showed intermediate learning abilities in both tasks compared to the parentals. Moreover, hybrids had slightly higher phenotypic dispersion, new trait combinations occurred in some hybrid individuals, and the mean phenotype of one hybrid group deviated away from the axis of variation of the parentals. Our method should hence be useful in further exploring how hybridization, and other evolutionary processes, impact behavioural and cognitive traits. Our results suggest that hybridization may promote cognitive variation and generate new trait combinations, even when learning performance at the group level is intermediate between parentals.

The effect of experimental hybridization on cognition and brain anatomy: limited phenotypic variation and transgression in Poeciliidae

“…To address this empirical gap, here we investigated the effect of hybridization on brain anatomy, learning ability, and cognitive flexibility in F1 and F2 hybrids of two closely related fish species (Poecilia reticulata and P. wingei). Our previous study of learning ability and cognitive flexibility in F1 females of this cross showed that female hybrids had slightly higher phenotypic dispersion, some hybrid individuals had transgressive trait scores, and the mean phenotype of one hybrid group deviated away from the axis of variation of the parentals, suggesting that hybridization may promote cognitive variation and generate new trait combinations (Vila Pouca et al 2022). These results on F1 female hybrids provided an important first test of whether hybridization can promote cognitive variation, a prerequisite for hybrids to have cognitive innovation potential (Seehausen 2013;Selz and Seehausen 2019).…”

“…Common guppy (Poecilia reticulata) populations descended from wild individuals from the upper Aripo river, Trinidad, and Endler's guppy (P. wingei) populations descended from wild individuals from Cumaná, Venezuela in 2006. Experimental fish were produced according to standard hybridization methods (Stelkens et al 2009;Vila Pouca et al 2022). In brief, non-hybrid (parental) crosses and reciprocal first-generation (F1) hybrids (i.e., P. reticulata females crossed with P. wingei males, and P. wingei females crossed with P. reticulata males) were bred simultaneously, in January and August 2020.…”

“…All groups of fish were bred and raised in identical conditions in a common garden environment and examined for brain morphology or cognitive traits at approximately one year of age. In the F1 cohort, F1 hybrids and parental offspring were obtained each from 12-16 families (Vila Pouca et al 2022). In the F2 cohort, F2 hybrids were obtained each from 16 families and parental offspring each from 10-12 families.…”

“…Females were tested in a colour discrimination assay that tests associative learning and in a reversal learning assay that tests cognitive flexibility, using red and yellow as stimulus colours (Fig. 1a,b;Buechel et al 2018;Fuss and Witte 2019;Vila Pouca et al 2022). F1 and parental females were tested with this assay in a previous study; detailed methods and results are given in Vila Pouca et al (2022), and those data are included here as part of this larger study.…”

“…1a,b;Buechel et al 2018;Fuss and Witte 2019;Vila Pouca et al 2022). F1 and parental females were tested with this assay in a previous study; detailed methods and results are given in Vila Pouca et al (2022), and those data are included here as part of this larger study. For the present study, F2 and parental females were tested in Sep-Oct. 2021.…”