A large and diverse autosomal haplotype is associated with sex-linked colour polymorphism in the guppy.

Male colour patterns of the Trinidadian guppy (Poecilia reticulata) are typified by extreme variation governed by both natural and sexual selection. Since guppy colour patterns are often inherited faithfully from fathers to sons, it has been hypothesised that many of the colour trait genes must be physically linked to sex determining loci as a 'supergene' on the sex chromosome. Here, we phenotype and genotype four guppy 'Iso-Y lines', where colour was inherited along the patriline for 40 generations. Using an unbiased phenotyping method, we confirm the breeding design was successful in creating four distinct colour patterns. We find that genetic differentiation among the Iso-Y lines is repeatedly associated with a diverse haplotype on an autosome (LG1), not the sex chromosome (LG12). Moreover, the LG1 haplotype exhibits elevated linkage disequilibrium and evidence of sex-specific diversity in the natural source population. We hypothesise that colour pattern polymorphism is driven by Y-autosome epistasis.

Kin Recognition in Guppies Uses Self-Referencing Based on Olfactory Cues.

AbstractKin recognition plays an important role in social behavior and evolution, but the proximate mechanisms by which individuals recognize kin remain poorly understood. In many species, individuals form a "kin template" that they compare with conspecifics' phenotypes to assess phenotypic similarity-and, by association, relatedness. Individuals may form a kin template through self-inspection (i.e., self-referencing) and/or by observing their rearing associates (i.e., family referencing). However, despite much interest, few empirical studies have successfully disentangled self-referencing and family referencing. Here, we employ a novel set of breeding crosses using the Trinidadian guppy (Poecilia reticulata) to disentangle referencing systems by manipulating exposure to kin from conception onward. We show that guppies discriminate among their full and maternal half siblings, which can be explained only by self-referencing. Additional behavioral experiments revealed no evidence that guppies incorporate the phenotypes of their broodmates or mother into the kin template. Finally, by manipulating the format of our behavioral tests, we show that olfactory communication is both necessary and sufficient for kin discrimination. These results provide robust evidence that individuals recognize kin by comparing the olfactory phenotypes of conspecifics with their own. This study resolves key questions about the proximate mechanisms underpinning kin recognition, with implications for the ontogeny and evolution of social behavior.

Experimentally altered male mating behaviour affects offspring exploratory behaviour via nongenetic paternal effects.

Evidence is emerging that fathers can have nongenetic effects on the phenotypes of their offspring. Most studies have focused on the role that nongenetic modifications to sperm can have on offspring phenotype; however, fathers can also have nongenetic effects on offspring through their interactions with females, called female-mediated paternal effects. These effects can occur in situations where male phenotype, e.g. behaviour or morphology, affects female stress and/or provisioning of offspring. These effects are potentially widespread, but few studies have explicitly investigated the role of female-mediated paternal effects on offspring phenotype. Here, we asked if male mating interactions can affect offspring via female mediated paternal effects in the Trinidadian guppy, Poecilia reticulata. To do this, we manipulated mating behaviour by: (i) administering a drug known to affect the neurotransmitter dopamine, and (ii) varying the familiarity of potential mates, which affects attractiveness in this species. With these treatments, we successfully manipulated the mating behaviour of male guppies and female preference for those males. Further, we found significant effects of sire mating behaviour, sire drug treatment, and parental familiarity status on behavioural measures of offspring anxiety in response to a novel object. Because Control offspring of 'familiar' and 'unfamiliar' pairs differed in their behaviour, our results cannot be solely attributed to potential nongenetic modifications to sperm caused by the drug. These results emphasize the importance of female-mediated paternal effects, including those caused by altered male mating behaviour, in shaping offspring phenotype.

Mating Preference for Novel Phenotypes Can Be Explained by General Neophilia in Female Guppies.

AbstractUnderstanding how genetic variation is maintained in ecologically important traits is a fundamental question in evolutionary biology. Male Trinidadian guppies (Poecilia reticulata) exhibit extreme genetic diversity in color patterns within populations, which is believed to be promoted by a female mating preference for rare or novel patterns. However, the origins of this preference remain unclear. Here, we test the hypothesis that mating preference for novel phenotypes is a by-product of general neophilia that evolved in response to selection in nonmating contexts. We measured among-female variation in preference for eight different, novel stimuli that spanned four ecological contexts: mate choice, exploration, foraging, and social (but nonsexual) interactions. Females exhibited preference for novelty in six out of eight tests. Individual variation in preference for novelty was positively correlated among all eight types of stimuli. Furthermore, factor analysis revealed a single axis of general neophilia that accounts for 61% of individual variation in preference for novel color patterns. The single-factor structure of neophilia suggests that interest in novelty is governed primarily by shared processes that transcend context. Because neophilia likely has a sizable heritable component, our results provide evidence that mating preference for novel phenotypes may be a nonadaptive by-product of natural selection on neophilia.

Males optimally balance selfish and kin-selected strategies of sexual competition in the guppy.

Resolving the strategies by which organisms compete for limited resources is key to understanding behavioural and social evolution. When competing for matings, males in many species allocate mating effort preferentially towards higher-quality females. How males balance this against avoiding competition with rival males, who should also prefer high-quality females, is poorly understood. Kin selection theory further complicates these dynamics: males should avoid competition with close relatives especially because of added, indirect fitness costs. However, whether between-male relatedness modulates the intensity of intrasexual competition is equivocal. Here, we develop and test an analytical model describing how males should optimally allocate their mating efforts in response to information about differences in female quality, competitor presence/absence and competitor relatedness. Using freely interacting groups of Trinidadian guppies (Poecilia reticulata), we show concordance between observed and predicted mating effort allocation across all combinations of these factors. Thus, male mating effort is sensitive to variation in female quality, competitor presence and competitor relatedness, which is consistent with a kin-selected strategy of male-male competition. The fit of our model's predictions demonstrates that males integrate assessments of female quality and competitive context in a quantitatively meaningful way, implicating a competitive strategy that has been fine-tuned to maximize inclusive fitness gains.