The quest for good genes: Epigamic traits, fitness, MHC and multilocus heterozygosity in the guppy.

The 'good genes' hypothesis for the evolution of male secondary sexual traits poses that female preferences for such traits are driven by indirect genetic benefits. However, support for the hypothesis remains ambiguous, and, in particular, the genetic basis for the benefits has rarely been investigated. Here, we use seminatural populations of Trinidadian guppies to investigate whether sexually selected traits (orange, black and iridescent colouration, gonopodium length and body size) predict fitness measured as the number of grandoffspring, a metric that integrates across fitness components and sexes. Furthermore, we tested whether two potential sources of genetic benefits-major histocompatibility complex (MHC) genotypes and multilocus heterozygosity (MLH)-are significant predictors of fitness and of the size of sexually selected traits. We found a significant, nonlinear effect of the area of black pigmentation and male body size on the number of grandoffspring, suggesting stabilizing selection on black area, and nonlinear selection favouring small body size. MLH was heritable (h2 = 0.14) and significantly predicted the number of grandoffspring, indicating the potential for genetic benefits based on heterozygosity. We also found support for local heterozygosity effects, which may reflect a noneven distribution of genetic load across the genome. MHC genotype was not significantly associated with any tested fitness component, or with the load of Gyrodactylus parasites. Neither MHC nor MLH was significant predictor of sexually selected traits. Overall, our results highlight the role of heterozygosity in determining fitness, but do not provide support for male sexually selected traits being indicators of genetic quality.

Can female guppies learn to like male colours? A test of the role of associative learning in originating sexual preferences.

How do female sexual preferences for male ornamental traits arise? The developmental origins of female preferences are still an understudied area, with most explanations pointing to genetic mechanisms. One intriguing, little-explored, alternative focuses on the role of associative learning in driving this process. According to this hypothesis, a preference learned in an ecological context can be transferred into a sexual context, resulting in changes in mating preferences as a by-product. I tested this hypothesis by first training female guppies to associate either orange or black colour with food delivery; I then presented videos of males with computer-manipulated coloured spots and measured female preference towards them. I also allowed females from both treatments to mate with males differing in their ratio of orange-to-black spots and measured the males' reproductive success. After training, female sexual preferences significantly diverged among treatments in the expected direction. In addition, orange males sired a greater proportion of offspring with females food-conditioned on orange compared to those conditioned on black. These results show that mating preferences can arise as a by-product of associative learning, which, via translation into variation in male fitness, can become associated with indirect genetic benefits, potentially leading to further evolution.

What do orange spots reveal about male (and female) guppies? A test using correlated responses to selection.

Female preferences for male ornamental traits can arise from indirect benefits, such as increased attractiveness or better viability of progeny, but empirical evidence for such benefits is inconsistent. Artificial selection offers a powerful way to investigate indirect effects of male ornaments. Here, we selected for the area of orange spots on male guppies, a trait subject to female preferences in our population, in replicated up- and down-selected lines. We found a significant direct response to selection, and a correlated response in female preferences, with females from down-selected lines showing less interest in more orange males. Nevertheless, up-selected males sired more offspring in direct competition with low-selected males, irrespective of female origin. We did not find a significantly correlated response to selection among any other fitness correlates we measured. Our results imply that female preferences for orange spots can lead to increased reproductive success of their sons, with no effect on general viability of progeny. Furthermore, although we demonstrate that female preferences may evolve via linkage disequilibrium with the preferred trait, the potential for runaway selection by positive feedback may be constrained by the lack of corresponding linkage with male reproductive competitiveness.

Balancing selection versus allele and supertype turnover in MHC class II genes in guppies.

Selection pressure from parasites is thought to be a major force shaping the extreme polymorphism of the major histocompatibility complex (MHC) genes, but the modes and consequences of selection remain unclear. Here, we analyse MHC class II and microsatellite diversity in 16 guppy (Poecilia reticulata) populations from two islands (Trinidad and Tobago) that have been separated for at least 10 ky. Within-population MHC diversity was high, but allele sharing was limited within islands and even lower between islands, suggesting relatively fast turnover of alleles. Allelic lineages strongly supported in phylogenetic analyses tended to be island-specific, suggesting rapid lineage sorting, and an expansion of an allelic lineage private to Tobago was observed. New alleles appear to be generated locally at a detectably high frequency. We did not detect a consistent signature of local adaptation, but FST outlier analysis suggested that balancing selection may be the more general process behind spatial variation in MHC allele frequencies in this system, particularly within Trinidad. We found no evidence for divergent allele advantage within populations, or for decreased genetic structuring of MHC supertypes compared to MHC alleles. The dynamic and complex nature of MHC evolution we observed in guppies, coupled with some evidence for balancing selection shaping MHC allele frequencies, are consistent with Red Queen processes of host-parasite coevolution.

Temperature increase altered Daphnia community structure in artificially heated lakes: a potential scenario for a warmer future.

Under conditions of global warming, organisms are expected to track their thermal preferences, invading new habitats at higher latitudes and altitudes and altering the structure of local communities. To fend off potential invaders, indigenous communities/populations will have to rapidly adapt to the increase in temperature. In this study, we tested if decades of artificial water heating changed the structure of communities and populations of the Daphnia longispina species complex. We compared the species composition of contemporary Daphnia communities inhabiting five lakes heated by power plants and four non-heated control lakes. The heated lakes are ca. 3-4 °C warmer, as all lakes are expected to be by 2100 according to climate change forecasts. We also genotyped subfossil resting eggs to describe past shifts in Daphnia community structure that were induced by lake heating. Both approaches revealed a rapid replacement of indigenous D. longispina and D. cucullata by invader D. galeata immediately after the onset of heating, followed by a gradual recovery of the D. cucullata population. Our findings clearly indicate that, in response to global warming, community restructuring may occur faster than evolutionary adaptation. The eventual recolonisation by D. cucullata indicates that adaptation to novel conditions can be time-lagged, and suggests that the long-term consequences of ecosystem disturbance may differ from short-term observations.

Bolder guppies do not have more mating partners, yet sire more offspring.

BACKGROUND: Intra-individual stable but inter-individually variable behaviours, i.e. personalities, are commonly reported across diverse animal groups, yet the reasons for their maintenance remain controversial. Therefore, studying fitness consequences of personality traits is necessary to discriminate between alternative explanations. RESULTS: Here, I measured boldness, a highly repeatable personality trait, and reproductive success in male guppies, Poecilia reticulata. I found that bolder males had higher reproductive success than their shyer conspecifics and they sired offspring with females who had larger clutches. CONCLUSIONS: This result provides direct evidence for fitness consequences of boldness in the guppy. It suggests that the effect may be driven by bolder males mating with more fecund females.

Does inbreeding affect personality traits?

The question of why variation is maintained in personality traits is an evolutionary puzzle. According to the condition-dependence hypothesis, such traits depend on condition, which limits the behavioral choices available to individuals. Because condition is affected by many genes, it can effectively be manipulated by inbreeding, which exposes the effects of deleterious recessive mutations. Here, I compared two personality traits, boldness and tendency to explore, of male guppies (Poecilia reticulata) from first-generation inbred and outbred treatments. Boldness in guppies is associated with increased sexual attractiveness and is thus expected to affect fitness. Therefore, I hypothesized that the personality traits would be negatively affected by inbreeding. However, the results indicated that inbred guppies did not differ in either personality trait from their outbred counterparts. This finding suggests that mechanisms other than condition dependence are maintaining personality variation in the guppy.

Immunogenetic novelty confers a selective advantage in host-pathogen coevolution.

The major histocompatibility complex (MHC) is crucial to the adaptive immune response of vertebrates and is among the most polymorphic gene families known. Its high diversity is usually attributed to selection imposed by fast-evolving pathogens. Pathogens are thought to evolve to escape recognition by common immune alleles, and, hence, novel MHC alleles, introduced through mutation, recombination, or gene flow, are predicted to give hosts superior resistance. Although this theoretical prediction underpins host-pathogen "Red Queen" coevolution, it has not been demonstrated in the context of natural MHC diversity. Here, we experimentally tested whether novel MHC variants (both alleles and functional "supertypes") increased resistance of guppies (Poecilia reticulata) to a common ectoparasite (Gyrodactylus turnbulli). We used exposure-controlled infection trials with wild-sourced parasites, and Gyrodactylus-naïve host fish that were F2 descendants of crossed wild populations. Hosts carrying MHC variants (alleles or supertypes) that were new to a given parasite population experienced a 35-37% reduction in infection intensity, but the number of MHC variants carried by an individual, analogous to heterozygosity in single-locus systems, was not a significant predictor. Our results provide direct evidence of novel MHC variant advantage, confirming a fundamental mechanism underpinning the exceptional polymorphism of this gene family and highlighting the role of immunogenetic novelty in host-pathogen coevolution.