Behavioural trait assortment in a social network: Patterns and implications

This a post-print, author-produced version of an article accepted for publication in Behavioral Ecology and Sociobiology. Copyright © 2009 Springer Verlag. The definitive version is available at http://link.springer.com/article/10.1007%2Fs00265-009-0802-x#The social fine structure of a population plays a central role in ecological and evolutionary processes. Whilst many studies have investigated how morphological traits such as size affect social structure of populations, comparatively little is known about the influence of behaviours such as boldness and shyness. Using information on social interactions in a wild population of Trinidadian guppies (Poecilia reticulata), we construct a social network. For each individual in the network, we quantify its behavioural phenotype using two measures of boldness, predator inspection tendency, a repeatable and reliably measured behaviour well studied in the context of co-operation, and shoaling tendency. We observe striking heterogeneity in contact patterns, with strong ties being positively assorted and weak ties negatively assorted by our measured behavioural traits. Moreover, shy fish had more network connections than bold fish and these were on average stronger. In other words, social fine structure is strongly influenced by behavioural trait. We assert that such structure will have implications for the outcome of selection on behavioural traits and we speculate that the observed positive assortment may act as an amplifier of selection contributing to the maintenance of co-operation during predator inspection

Evolution of non-kin cooperation: social assortment by cooperative phenotype in guppies

This is the final version. Available from The Royal Society via the DOI in this record.Data accessibility: The data used in this study are available at the Dryad Digital Repository: doi:10.5061/dryad.js446q8Cooperation among non-kin constitutes a conundrum for evolutionary biology. Theory suggests that non-kin cooperation can evolve if individuals differ consistently in their cooperative phenotypes and assort socially by these, such that cooperative individuals interact predominantly with one another. However, our knowledge of the role of cooperative phenotypes in the social structuring of real-world animal populations is minimal. In this study, we investigated cooperative phenotypes and their link to social structure in wild Trinidadian guppies (Poecilia reticulata). We first investigated whether wild guppies are repeatable in their individual levels of cooperativeness (i.e. have cooperative phenotypes) and found evidence for this in seven out of eight populations, a result which was mostly driven by females. We then examined the social network structure of one of these populations where the expected fitness impact of cooperative contexts is relatively high, and found assortment by cooperativeness, but not genetic relatedness. In contrast, in accordance with our expectations we did not find assortment by cooperativeness in a population where the expected fitness impact of cooperative contexts is lower. Our results provide empirical support for current theory and suggest that assortment by cooperativeness is important for the evolution and persistence of non-kin cooperation in real-world populations.Leverhulme TrustDanish Council for Independent Researc

Phenotypic Plasticity in Response to the Social Environment: Effects of Density and Sex Ratio on Mating Behaviour Following Ecotype Divergence

The ability to express phenotypically plastic responses to environmental cues might be adaptive in changing environments. We studied phenotypic plasticity in mating behaviour as a response to population density and adult sex ratio in a freshwater isopod (Asellus aquaticus). A. aquaticus has recently diverged into two distinct ecotypes, inhabiting different lake habitats (reed Phragmites australis and stonewort Chara tomentosa, respectively). In field surveys, we found that these habitats differ markedly in isopod population densities and adult sex ratios. These spatially and temporally demographic differences are likely to affect mating behaviour. We performed behavioural experiments using animals from both the ancestral ecotype (“reed” isopods) and from the novel ecotype (“stonewort” isopods) population. We found that neither ecotype adjusted their behaviour in response to population density. However, the reed ecotype had a higher intrinsic mating propensity across densities. In contrast to the effects of density, we found ecotype differences in plasticity in response to sex ratio. The stonewort ecotype show pronounced phenotypic plasticity in mating propensity to adult sex ratio, whereas the reed ecotype showed a more canalised behaviour with respect to this demographic factor. We suggest that the lower overall mating propensity and the phenotypic plasticity in response to sex ratio have evolved in the novel stonewort ecotype following invasion of the novel habitat. Plasticity in mating behaviour may in turn have effects on the direction and intensity of sexual selection in the stonewort habitat, which may fuel further ecotype divergence

Sperm transfer through forced matings and its evolutionary implications in natural guppy (Poecilia reticulata) populations

Abstract: In species in which individuals alternate between mating strategies, males may respond to elevated predation risk by switching from conspicuous courtship displays to less risky or more profitable sneaky mating attempts. As a consequence, in such species female choice is likely to be undermined more frequently in relatively dangerous localities. We tested this prediction using the guppy, a species of fish in which individual males alternate between courtship (solicited) and forced (unsolicited) copulations according to prevailing levels of predation. We collected females at late stages of gestation from four high- and four low-predation populations in Trinidad and examined them for the presence of sperm in their gonoducts. Due to the patterns of sperm storage in guppies, sperm found in the gonoducts of such late-cycle females can only arise from unsolicited copulations. We anticipated that because female guppies are subject to greater sexual harassment in the form of forced mating attempts in high-risk localities, a higher proportion of females in these populations would contain sperm in their gonoducts arising from recent unsolicited copulations. Contrary to this prediction, only one of the four paired comparisons (from the Quare River) revealed a significant difference in the proportion of females recently inseminated through forced copulations. The paired comparisons for the remaining three rivers revealed no significant differences in the proportion of females with recoverable sperm in their gonoducts. However, overall, we found that 44.5% ( +/- 4.3 SE) of females had sperm in their gonoduct arising from sneaky mating, a figure three times higher than previously reported for this species. We discuss these findings in relation to recent predictions concerning the strength of sexual selection in natural populations

Back to school:can antipredator behaviour in guppies be enhanced through social learning?

The ability to recognize and respond to predators often has a learned component, but few studies have examined the role of social learning in the development of antipredator behaviour. We investigated whether wild-caught juvenile guppies, Poecilia reticulata, from a low-predation river in Trinidad increase their response towards a novel predator through association with conspecifics from a high-predation river. We assigned fish to one of three treatment groups: (1) repeated exposure to a model accompanied by high-predation conspecifics; (2) repeated exposure to a model with low-predation conspecifics; (3) a control group in which focal fish interacted with high-predation fish in the absence of the model. Guppies trained with high-predation, but not low-predation, 'demonstrators' significantly improved their antipredator behaviour (spent more time schooling and inspected the model from further away). The guppies assigned to the control group showed no significant improvement in antipredator behaviour after the training period, suggesting that association with experienced conspecifics in the absence of the model is not sufficient to enhance the antipredator behaviour of naive fish. We conclude that guppies can improve their antipredator behaviour through association with more experienced conspecifics in the presence of visual cues simulating high predation risk. (C) 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.</p

Genetic detection of forced copulations between sympatric populations of Poecilia reticulata and Poecilia picta.

The reproductive success of the sneaky mating tactic is difficult to determine in fish with internal fertilization. We approached this problem by developing an assay that allows the recovery of sperm DNA from the reproductive tract of females. This assay was used to test whether sperm transfer occurs between sympatric populations of the guppy, Poecilia reticulata, and its putative sister species, Poecilia picta. Six hundred females of both species from two sympatric sites in Trinidad were collected, and then the contents of the females' reproductive tracts were analysed using reciprocally diagnostic microsatellite markers. Conspecific sperm occurred in approximately 86% of females, whereas heterospecific sperm were found in only 4% of females. Because females of either species do not mate willingly with heterospecific males, the results indicate that sneaky mating results in the transfer of sperm. The data are consistent with the idea that sexual conflict can result in differences in the strength of behavioural isolation between the sexes, and they suggest that behavioural isolation is unlikely to have driven speciation between the guppy and P. picta. (c) 2006 The Linnean Society of London.</p

Sensory-based quantification of male colour patterns in Trinidadian guppies reveals no support for parallel phenotypic evolution in multivariate trait space

This is the final version. Available from Wiley via the DOI in this record. Phenotypic data, SNP data sets, R and Java scripts have been made available on Dryad (doi.org/10.5061/dryad.s1rn8pk83), and genomic data (raw fastq files) are under ENA Project Accession PRJEB45804.Parallel evolution, in which independent populations evolve along similar phenotypic trajectories, offers insights into the repeatability of adaptive evolution. Here, we revisit a classic example of parallelism, that of repeated evolution of brighter males in the Trinidadian guppy (Poecilia reticulata). In guppies, colonisation of low predation habitats is associated with emergence of 'more colourful' phenotypes since predator-induced viability selection for crypsis weakens while sexual selection by female preference for conspicuousness remains strong. Our study differs from previous investigations in three respects. First, we adopted a multivariate phenotyping approach to characterise parallelism in multitrait space. Second, we used ecologically-relevant colour traits defined by the visual systems of the two selective agents (i.e., guppy, predatory cichlid). Third, we estimated population genetic structure to test for adaptive (parallel) evolution against a model of neutral phenotypic divergence. We find strong phenotypic differentiation that is inconsistent with a neutral model but very limited support for the predicted pattern of greater conspicuousness at low predation. Effects of predation regime on each trait were in the expected direction, but weak, largely nonsignificant, and explained little among-population variation. In multitrait space, phenotypic trajectories of lineages colonising low from high predation regimes were not parallel. Our results are consistent with reduced predation risk facilitating adaptive differentiation, potentially by female choice, but suggest that this proceeds in independent directions of multitrait space across lineages. Pool-sequencing data also revealed SNPs showing greater differentiation than expected under neutrality, among which some are found in genes contributing to colour pattern variation, presenting opportunities for future genetic study.Biotechnology & Biological Sciences Research Council (BBSRC)European Research Council (ERC

Sex ratio dynamics and fluctuating selection pressures in natural populations of the Trinidadian guppy, Poecilia reticulata

In many species, population sex ratios have far-reaching consequences for a wide variety of population-level and behavioural processes and can directly influence sexual selection through differential effects on male and female mating behaviour. Although sex ratios are often treated as more or less stable population characteristics, recent theoretical evidence suggests that sex ratios fluctuate under many conditions, and that the amplitude of these fluctuations can be considerable. Few studies have attempted to quantify this variation in systems with prominent, sex ratio-dependent sexual conflict. One of the species with the greatest potential to integrate these factors in the wild is the Trinidadian guppy, Poecilia reticulata. In this study, we quantified natural sex ratio variation both as detailed longitudinal studies of focal guppy populations and as snapshot estimates across a range of freshwater habitats. In line with theoretical predictions, we expected to detect significant sex ratio variation over time. We also investigated the association between juvenile and adult sex ratios to quantify a possible compensatory feedback implied in standard models of sex ratio evolution. Our results confirm that population-level sex ratios in wild guppy populations have a range of dynamic features, with all four focal populations showing significant variation in sex ratio over time. The survey showed that juveniles were generally close to equal (50:50) sex ratios whereas 7 out of 11 adult sex ratios differed significantly from equality. We found no evidence that a surplus of juveniles of the locally rarer sex had been produced. The results indicate that sex ratios and hence the balance between sexual selection and sexual coercion is normally fluctuating in nature, despite juvenile ratios being close to equality