Heritable variation in colour patterns mediating individual recognition

Abstract

Understanding the developmental and evolutionary processes that generate and maintain variation in natural populations remains a major challenge for modern biology. Populations of Polistes fuscatus paper wasps have highly variable colour patterns that mediate individual recognition. Previous experimental and comparative studies have provided evidence that colour pattern diversity is the result of selection for individuals to advertise their identity. Distinctive identity-signalling phenotypes facilitate recognition, which reduces aggression between familiar individuals in P. fuscatus wasps. Selection for identity signals may increase phenotypic diversity via two distinct modes of selection that have different effects on genetic diversity. Directional selection for increased plasticity would greatly increase phenotypic diversity but decrease genetic diversity at associated loci. Alternatively, heritable identity signals under balancing selection would maintain genetic diversity at associated loci. Here, we assess whether there is heritable variation underlying colour pattern diversity used for facial recognition in a wild population of P. fuscatus wasps. We find that colour patterns are heritable and not Mendelian, suggesting that multiple loci are involved. Additionally, patterns of genetic correlations among traits indicated that many of the loci underlying colour pattern variation are unlinked and independently segregating. Our results support a model where the benefits of being recognizable maintain genetic variation at multiple unlinked loci that code for phenotypic diversity used for recognition.

Signal function drives phenotypic and genetic diversity: the effects of signalling individual identity, quality or behavioural strategy

“…Identity signals are predicted to occur as fixed phenotypes with high degrees of genetic determination [5]. The few parent -offspring analyses that have been conducted on individual identity signals demonstrate high heritability [17,19].…”

“…Identity signals are predicted to occur as fixed phenotypes with high degrees of genetic determination [5]. The few parent -offspring analyses that have been conducted on individual identity signals demonstrate high heritability [17,19]. Additionally, identity signals are expected to have low costs associated with their production and maintenance because phenotypes that are not costly will spread to a higher equilibrium frequency than more costly phenotypes [5].…”

Visual and chemical signals provide different information in Polistes fuscatus wasps

“…Color patterns were not experimentally altered. Previous work has found that P. fuscatus color patterns tend to be more similar within nests than between nests (Sheehan et al., 2017).…”

“…Because wasps learn the unique facial patterns of each nestmate, they could potentially use facial patterns to discriminate between nestmates with known facial patterns and non‐nestmates with novel facial patterns. Further, nestmates tend to have more similar facial patterns than non‐nestmates, though there is still extensive facial pattern variation within each nest (Sheehan et al., 2017). Integrating information from both visual and chemical signals during nestmate recognition could enable wasps to make more accurate assessments about nestmate identity than relying on a chemical signals alone.…”

Estimating heritability in honeybees: Comparison of three major methods based on empirical and simulated datasets

“…Similarly, in sex chromosome, genes linked to the X-chromosome are transmitted to daughters and sons, whereas genes linked to the Y-chromosomes are only transmitted to sons. This method of matrix inversion is implemented in the R package nadiv (Wolak, 2012), which has been applied to wasps but never to honeybees (Sheehan et al, 2017). However, many traits under selection are genetically correlated and will not evolve independently from each other, due to linkage or pleiotropy (one loci influencing several traits).…”