Parental care behaviour in response to perceived paternity is not mediated by 11-ketotestosterone in bluegill sunfish.

Parental care is critical for the survival of many young animals, but parental care can be costly to the individual providing care. To balance this cost, parents can allocate their care to offspring based on their value, which can be dependent on the offspring's relatedness to the parent. Bluegill (Lepomis macrochirus) is a fish characterized by uniparental male care and high levels of cuckoldry. While parental males of this species have been shown to adaptively adjust their care in response to paternity, the mechanisms for this adjustment are not well understood. Androgens are steroid hormones that are associated with parental care behaviours in many species including bluegill. Here, we test the hypothesis that circulating androgen concentrations mediate the adjustment in care provided by bluegill parental males by manipulating perceived paternity and then measuring circulating 11-ketotestosterone concentration and parental care behaviour. We show that males with higher perceived paternity provide higher levels of nurturing and nest defense behaviour, but contrary to expectations, we found that these males had lower concentrations of 11-ketotestosterone. Furthermore, we found positive correlations between individual circulating plasma 11-ketotestosterone concentrations and nurturing behaviour, but not with the aggressive behaviours that differed between paternity treatments. While bluegill make behavioural changes in response to perceived paternity, these changes do not appear to be modulated by 11-ketotestosterone.

Evolution of kin recognition mechanisms in a fish.

Both selection and phylogenetic history can influence the evolution of phenotypic traits. Here we used recently characterized variation in kin recognition mechanisms among six guppy populations to explore the phylogenetic history of this trait. Guppies can use two different kin recognition mechanisms: either phenotype matching, in which individuals are identified based on comparison with a recognition template, or familiarity, in which individuals are remembered based on previous interactions. Across the six populations, we identified four transitions in recognition mechanism: phenotype matching evolved once and was subsequently lost in a single population, whereas familiarity evolved twice. Based on a molecular clock, these transitions occurred among populations that had diverged on a timescale of hundreds of thousands of years, which is two orders of magnitude faster than previously documented transitions in recognition mechanisms. A randomization test provided no evidence that recognition mechanisms were constrained by phylogeny, suggesting that recognition mechanisms have the capacity to evolve rapidly, although the specific selection pressures that may be contributing to variation in recognition mechanisms across populations remain unknown.

Multiple paternity and kin recognition mechanisms in a guppy population.

Help directed toward kin (nepotism) is an important example of social behaviour. Such helping behaviour requires a mechanism to distinguish kin from nonkin. The prevailing kin recognition hypothesis is that when familiarity is a reliable cue of relatedness, other mechanisms of recognition will not evolve. However, when familiarity is an unreliable cue of relatedness, kin recognition by phenotype matching is instead predicted to evolve. Here we use genetic markers to show that guppies (Poecilia reticulata) from a population in a tributary of the Paria River in Trinidad are characterized by a high degree of multiple mating with 95% of broods having more than one sire and some dams having offspring sired by six males. These levels of multiple mating are the highest reported among live-bearing fishes. The mean relatedness of brood-mates was 0.36 (as compared to 0.5 for full-siblings). Therefore, familiarity does not seem to be a reliable mechanism to assess full-sibling relatedness. Using two-choice behavioural trials, we found that juveniles from this population use both phenotype matching and familiarity to distinguish kin from nonkin. However, we did not find strong evidence that the guppies use these mechanisms to form shoals of related individuals as adults, which is similar to results from other guppy populations in Trinidad. The use of both familiarity and phenotype matching is discussed in the context of the Paria River guppy population's mating system and ecology. Overall, these data provide support for the kin recognition hypothesis and increase our understanding of the evolution of kin recognition systems.

Promiscuity drives self-referent kin recognition.

Kin selection theory has been one of the most significant advances in our understanding of social behavior . However, the discovery of widespread promiscuity has challenged the evolutionary importance of kin selection because it reduces the benefit associated with helping nestmates . This challenge would be resolved if promiscuous species evolved a self-referent kin-recognition mechanism that enables individuals to differentiate kin and nonkin . Here, we take advantage of an asymmetry in the level of promiscuity among males of alternative life histories in the bluegill sunfish (Lepomis macrochirus). We show that, as a consequence of this asymmetry, offspring of "parental" males have a high level of relatedness to nestmates, whereas offspring of "cuckolder" males have a low level of relatedness to nestmates. We find that offspring of parentals do not use a direct recognition mechanism to discriminate among nestmates, whereas offspring of cuckolders use kin recognition by self-referent phenotype matching to differentiate between kin and nonkin. Furthermore, we estimate that the cost of utilizing such self-referent kin recognition is equivalent to a relatedness (R) of at least 0.06. These results provide compelling evidence for adaptive use of kin recognition by self-referent phenotype matching and confirm the importance of kinship in social behavior.