The genetics of niche-specific behavioral tendencies in an adaptive radiation of cichlid fishes.

Behavior is critical for animal survival and reproduction, and possibly for diversification and evolutionary radiation. However, the genetics behind adaptive variation in behavior are poorly understood. In this work, we examined a fundamental and widespread behavioral trait, exploratory behavior, in one of the largest adaptive radiations on Earth, the cichlid fishes of Lake Tanganyika. By integrating quantitative behavioral data from 57 cichlid species (702 wild-caught individuals) with high-resolution ecomorphological and genomic information, we show that exploratory behavior is linked to macrohabitat niche adaptations in Tanganyikan cichlids. Furthermore, we uncovered a correlation between the genotypes at a single-nucleotide polymorphism upstream of the AMPA glutamate-receptor regulatory gene cacng5b and variation in exploratory tendency. We validated this association using behavioral predictions with a neural network approach and CRISPR-Cas9 genome editing.

Natural variation in social conditions affects male mate choosiness in the amphipod Gammarus roeselii.

The extent of male mate choosiness is driven by a trade-off between various environmental factors associated with the costs of mate acquisition, quality assessment and opportunity costs. Our knowledge about natural variation in male mate choosiness across different populations of the same species, however, remains limited. In this study, we compared male mate choosiness across 10 natural populations of the freshwater amphipod Gammarus roeselii (Gervais 1835), a species with overall high male mating investments, and evaluated the relative influence of population density and sex ratio (both affecting mate availability) on male mate choosiness. We investigated amplexus establishment after separating mating pairs and presenting focal males with a novel, size-matched female from the same population. Our analysis revealed considerable effects of sex ratio and (to a lesser extent) population density on time until amplexus establishment (choosiness). Male amphipods are able to perceive variable social conditions (e.g., sex ratio) and modify their mating strategy accordingly: We found choosiness to be reduced in increasingly male-biased populations, whereas selectivity increases when sex ratio becomes female biased. With this, our study expands our limited knowledge on natural variations in male mate choosiness and illustrates the importance of sex ratio (i.e., level of competition) for male mating decisions in natural environments. Accounting for variation in sex ratios, therefore, allows envisioning a distinctive variation of choosiness in natural populations and highlights the importance of considering social background information in future behavioral studies.

Predator-induced changes of male and female mating preferences: innate and learned components.

While many mating preferences have a genetic basis, the question remains as to whether and how learning/experience can modify individual mate choice decisions. We used wild-caught (predator-experienced) and F1 laboratory-reared (predator-naïve) invasive Western mosquitofish Gambusia affinis from China to test whether mating preferences (assessed in a first mate choice test) would change under immediate predation threat. The same individuals were tested in a second mate choice test during which 1 of 3 types of animated predators was presented: 1) a co-occurring predator, 2) a co-evolved but not currently co-occurring predator, and 3) a non-piscivorous species as control. We compared preference scores derived from both mate choice tests to separate innate from experiential effects of predation. We also asked whether predator-induced changes in mating preferences would differ between sexes or depend on the choosing individual's personality type and/or body size. Wild-caught fish altered their mate choice decisions most when exposed to the co-occurring predator whereas laboratory-reared individuals responded most to the co-evolved predator, suggesting that both innate mechanisms and learning effects are involved. This behavior likely reduces individuals' risk of falling victim to predation by temporarily moving away from high-quality (i.e., conspicuous) mating partners. Accordingly, effects were stronger in bolder than shyer, large- compared with small-bodied, and female compared with male focal individuals, likely because those phenotypes face an increased predation risk overall. Our study adds to the growing body of literature appreciating the complexity of the mate choice process, where an array of intrinsic and extrinsic factors interacts during decision-making.

Consistent individual differences in associative learning speed are not linked to boldness in female Atlantic mollies.

Recent studies on consistent individual differences in behavioural tendencies (animal personality) raised the question of whether individual differences in cognitive abilities can be linked to certain personality types. We tested female Atlantic mollies (Poecilia mexicana) in two different classical conditioning experiments. For the first time, we provide evidence for highly consistent individual differences in associative learning speed in fish. We characterized the same individuals for boldness in two experimental situations (latency to emerge from shelter and freezing time after a simulated predator attack) and found high behavioural repeatability. When we tested for a potential correlation between associative learning speed and boldness, however, there was no evidence for a link between them. Our study design included several steps to avoid typical pitfalls of disadvantaging shy individuals during learning tests. We caution that other experimental studies may have suffered from erroneous interpretations due to a more cautious coping style of shy individuals in the respective setup used to assess learning.

Personality differentially affects individual mate choice decisions in female and male Western mosquitofish (Gambusia affinis).

Consistent individual differences in behavioral tendencies (animal personality) can affect individual mate choice decisions. We asked whether personality traits affect male and female mate choice decisions similarly and whether potential personality effects are consistent across different mate choice situations. Using western mosquitofish (Gambusia affinis) as our study organism, we characterized focal individuals (males and females) twice for boldness, activity, and sociability/shoaling and found high and significant behavioral repeatability. Additionally, each focal individual was tested in two different dichotomous mate choice tests in which it could choose between computer-animated stimulus fish of the opposite sex that differed in body size and activity levels, respectively. Personality had different effects on female and male mate choice: females that were larger than average showed stronger preferences for large-bodied males with increasing levels of boldness/activity (i.e., towards more proactive personality types). Males that were larger than average and had higher shoaling tendencies showed stronger preferences for actively swimming females. Size-dependent effects of personality on the strength of preferences for distinct phenotypes of potential mating partners may reflect effects of age/experience (especially in females) and social dominance (especially in males). Previous studies found evidence for assortative mate choice based on personality types or hypothesized the existence of behavioral syndromes of individuals' choosiness across mate choice criteria, possibly including other personality traits. Our present study exemplifies that far more complex patterns of personality-dependent mate choice can emerge in natural systems.

Predation risk and abiotic habitat parameters affect personality traits in extremophile populations of a neotropical fish (Poecilia vivipara).

Understanding whether and how ambient ecological conditions affect the distribution of personality types within and among populations lies at the heart of research on animal personality. Several studies have focussed on only one agent of divergent selection (or driver of plastic changes in behavior), considering either predation risk or a single abiotic ecological factor. Here, we investigated how an array of abiotic and biotic environmental factors simultaneously shape population differences in boldness, activity in an open-field test, and sociability/shoaling in the livebearing fish Poecilia vivipara from six ecologically different lagoons in southeastern Brazil. We evaluated the relative contributions of variation in predation risk, water transparency/visibility, salinity (ranging from oligo- to hypersaline), and dissolved oxygen. We also investigated the role played by environmental factors for the emergence, strength, and direction of behavioral correlations. Water transparency explained most of the behavioral variation, whereby fish from lagoons with low water transparency were significantly shyer, less active, and shoaled less than fish living under clear water conditions. When we tested additional wild-caught fish from the same lagoons after acclimating them to homogeneous laboratory conditions, population differences were largely absent, pointing toward behavioral plasticity as a mechanism underlying the observed behavioral differences. Furthermore, we found correlations between personality traits (behavioral syndromes) to vary substantially in strength and direction among populations, with no obvious associations with ecological factors (including predation risk). Altogether, our results suggest that various habitat parameters simultaneously shape the distribution of personality types, with abiotic factors playing a vital (as yet underestimated) role. Furthermore, while predation is often thought to lead to the emergence of behavioral syndromes, our data do not support this assumption.

Context-dependent female mate choice maintains variation in male sexual activity.

The existence of individual variation in males' motivation to mate remains a conundrum as directional selection should favour high mating frequencies. Balancing selection resulting from (context-dependent) female mate choice could contribute to the maintenance of this behavioural polymorphism. In dichotomous choice tests, mosquitofish (Gambusia holbrooki) females preferred virtual males showing intermediate mating frequencies, reflecting females' tendencies to avoid harassment by highly sexually active males. When tested in the presence of a female shoal-which protects females from male harassment-focal females showed significantly stronger preferences for high sexual activity. A trade-off between (indirect) benefits and (direct) costs of mating with sexually active males probably explains context-dependent female mate choice, as costs depend on the social environment in which females choose their mates. No preference was observed when we tested virgin females, suggesting that the behavioural pattern described here is part of the learned behavioural repertoire of G. holbrooki females.

Shared and unique patterns of phenotypic diversification along a stream gradient in two congeneric species.

Stream ecosystems show gradual variation of various selection factors, which can result in a zonation of species distributions and gradient evolution of morphological and life-history traits within species. Identifying the selective agents underlying such phenotypic evolution is challenging as different species could show shared and/or unique (species-specific) responses to components of the river gradient. We studied a stream gradient inhabited by two mosquitofishes (genus Gambusia) in the Río Grijalva basin in southern Mexico and found a patchy distribution pattern of both congeners along a stretch of 100 km, whereby one species was usually dominant at a given site. We uncovered both shared and unique patterns of diversification: some components of the stream gradient, including differences in piscine predation pressure, drove shared patterns of phenotypic divergence, especially in females. Other components of the gradient, particularly abiotic factors (max. annual temperature and temperature range) resulted in unique patterns of divergence, especially in males. Our study highlights the complexity of selective regimes in stream ecosystems. It exemplifies that even closely related, congeneric species can respond in unique ways to the same components of the river gradient and shows how both sexes can exhibit quite different patterns of divergence in multivariate phenotypic character suites.

Does personality affect premating isolation between locally-adapted populations?

BACKGROUND: One aspect of premating isolation between diverging, locally-adapted population pairs is female mate choice for resident over alien male phenotypes. Mating preferences often show considerable individual variation, and whether or not certain individuals are more likely to contribute to population interbreeding remains to be studied. In the Poecilia mexicana-species complex different ecotypes have adapted to hydrogen sulfide (H2S)-toxic springs, and females from adjacent non-sulfidic habitats prefer resident over sulfide-adapted males. We asked if consistent individual differences in behavioral tendencies (animal personality) predict the strength and direction of the mate choice component of premating isolation in this system. RESULTS: We characterized focal females for their personality and found behavioral measures of 'novel object exploration', 'boldness' and 'activity in an unknown area' to be highly repeatable. Furthermore, the interaction term between our measures of exploration and boldness affected focal females' strength of preference (SOP) for the resident male phenotype in dichotomous association preference tests. High exploration tendencies were coupled with stronger SOPs for resident over alien mating partners in bold, but not shy, females. Shy and/or little explorative females had an increased likelihood of preferring the non-resident phenotype and thus, are more likely to contribute to rare population hybridization. When we offered large vs. small conspecific stimulus males instead, less explorative females showed stronger preferences for large male body size. However, this effect disappeared when the size difference between the stimulus males was small. CONCLUSIONS: Our results suggest that personality affects female mate choice in a very nuanced fashion. Hence, population differences in the distribution of personality types could be facilitating or impeding reproductive isolation between diverging populations depending on the study system and the male trait(s) upon which females base their mating decisions, respectively.