Evidence for selfing in a vertebrate from whole-genome sequencing.

A growing number of recent genomic studies report asexual parthenogenetic reproduction in a wide range of taxa, including vertebrate species from the reptile, bird, and fish lineages. Yet, self-fertilization (selfing) has been recorded only in a single vertebrate, the mangrove killifish Kryptolebias marmoratus In cichlid fishes, sex determination is notably diverse and can be influenced by the environment, and sequential hermaphroditism has been reported for some species. Here, we present evidence for a case of facultative selfing in the cichlid fish Benitochromis nigrodorsalis, which is otherwise known as biparentally reproducing ovophilic mouthbrooder from Western Africa. Our laboratory observations revealed that a wild-caught individual produced repeatedly viable offspring in absence of a mating partner. By analyzing genome-wide single-nucleotide polymorphism (SNP) data, we compare that individual and two of its offspring to shed light on its reproductive mode. First, our results confirm uniparental reproduction. Second, overall heterozygosity is reduced in the offspring compared with outbred individuals. Retained maternal heterozygosity in the offspring is ∼51%, which is close to the theoretically expected value of a heterozygosity reduction of 50% by selfing. Heterozygosity patterns along individual chromosomes do not point to alternative parthenogenetic reproductive mechanisms like automixis by terminal or central fusion. Facultative selfing may represent an adaptive strategy ensuring reproduction when mating partners are absent and, hence, contribute to the cichlids' enormous evolutionary success.

Impact of genetic relatedness on reproductive behavior in Pelvicachromis pulcher, a biparental cichlid fish with mutual mate choice and ornamentation.

Inbreeding can result in inbreeding depression. Therefore, many species seek to avoid inbreeding. However, theory predicts that inbreeding can be beneficial. Accordingly, some species tolerate inbreeding or even prefer mating with close relatives. Evidence for active inbreeding, i.e., kin-mating preference was reported in the biparental African cichlid fish Pelvicachromis taeniatus. Related mating partners revealed better parental cooperation due to kin selection, a potential benefit of inbreeding. In this study, we investigated kin-mating preference in a genetically diverse, outbred F2-lab population of Pelvicachromis pulcher, a closely related species to P. taeniatus. Like P. taeniatus, this species shows mutual ornamentation and mate choice as well as intense biparental brood care. The F1 P. pulcher generation had revealed signs of inbreeding depression but no inbreeding avoidance. We studied mating behavior and aggression in trios consisting of a male P. pulcher, an unfamiliar sister, and an unfamiliar, unrelated female. Because the study focused on kin-mating patterns, female pairs were matched for body size and coloration. The results provide no evidence for inbreeding avoidance but rather suggest inbreeding preference. We also found no significant impact of inbreeding on offspring survival. The results suggest no inbreeding avoidance in P. pulcher; however, the strength of inbreeding preference and inbreeding depression seems to be variable. We discuss possible causes for this variation like context-dependent inbreeding depression. The number of eggs positively correlated with female body size and coloration. Furthermore, the female aggressiveness was positively correlated with female coloration indicating that coloration signal female dominance and quality.

Environmental habituation and sexual composition affect juveniles' shoaling activity in a cichlid fish (Pelvicachromis taeniatus).

Group living is widespread in animals, and many fishes form shoals. Examining within-group interactions in fishes may contribute to the general understanding of dynamic social structures in animals. The sex ratio of a group has been shown to influence grouping decisions of fishes and can be expected to affect behaviour at group level. Behavioural experiments usually involve relatively short acclimatisation times, although the establishment of environmental habituation in fishes is understudied. This study tests whether the sex ratio and long-term habituation to experimental conditions influence general shoal performance (activity parameters, density) and responses of shoals to an acoustic-mechanical disturbance cue in juveniles of the cichlid fish Pelvicachromis taeniatus via individual tracking. The disturbance consisted of a defined hit against the experimental tank, which caused sudden noise and water movement. We found that a higher proportion of females increases shoal activity (swimming speed and distance covered), suggesting that female P. taeniatus are more active than males. Furthermore, shoal activity declined when shoals habituated to the experimental settings and with the time that the shoals were grouped together, which may reflect intensified group member familiarity. Moreover, behavioural changes after disturbance were weaker when individuals were kept with their group longer and more familiar to the experimental conditions. For prey species, lower activity might be beneficial under natural conditions due to lower conspicuousness of the group. We did not find any significant effects of the investigated factors on shoal density (mean interindividual distance) and speed synchronisation. The results indicate that sexual composition, familiarity between shoal members and habituation to the experimental environment affect shoal performance in a cichlid fish.

Enhanced ambient UVB radiation affects post-mating, but not pre-mating sexual traits in a fish.

Organisms inhabiting shallow aquatic habitats currently experience increasing levels of solar ultraviolet B radiation (UVB). UVB causes damage on cellular and molecular levels and can affect associated life-history traits either through direct exposure or indirectly through oxidative stress generation. We examined UVB effects on pre- and post-mating sexual traits in three-spined stickleback fish (Gasterosteus aculeatus). Adult, reproductively non-active males were assigned to two exposure treatments under semi-natural conditions in an outdoor experiment; one group received natural radiation (UVBnormal) whilst the other group received additional UVB (UVBenhanced). After two months, colour metrics were used to quantify male breeding colouration as pre-mating trait. At the post-mating stage, sperm morphology, number and movement as well as testes mass were determined. Males did not significantly differ in sexual ornamentation between treatments, but UVBenhanced fish had smaller testes as well as fewer and shorter sperm than UVBnormal fish. Sperm movement was not significantly different between treatments. However, in UVBenhanced males, linear and progressive movement of sperm was positively correlated with sperm morphology (head-to-tail length ratio), whereas in UVBnormal males this relationship was negative (but not significant). Additionally, there was a significant treatment by body condition interaction concerning head-to-tail length ratio, i.e. head-to-tail length ratio increased with condition in UVBnormal males whereas there was no relationship in UVBenhanced fish. Our findings reveal that increased UVB levels influence post-mating fitness-relevant traits in males whilst having no significant impact on pre-mating sexual traits, suggesting selective UVB-effects at the gamete level with consequences for reproductive performance.

Long-term UVB exposure promotes predator-inspection behaviour in a fish.

Ultraviolet-B radiation (UVB) reaching the earth's surface has increased due to human-caused stratospheric ozone depletion. Whereas the harmful effects of UVB on aquatic organisms are well studied at the molecular and cellular level, recent studies have also begun to address behavioural changes caused by sublethal amounts of UVB. However, the behavioural consequences of long-term exposure to ecologically relevant UVB levels over several life stages are virtually unknown, particularly with regard to predator-prey behaviour. We found increased predator-inspection behaviour together with a smaller body length in three-spined sticklebacks (Gasterosteus aculeatus) after fish were exposed for about seven months to natural sunlight conditions with enhanced UVB, compared with full siblings exposed to natural sunlight only. The observed change in antipredator behaviour may reflect a direct behavioural response mediated through UVB-induced oxidative stress during development. Alternatively, the smaller body size in UVB-exposed fish may result in an increased inspection effort allowing them to spend more time foraging. Our findings suggest that, within the scope of environmental change, UVB radiation constitutes an important stress factor by eliciting behavioural responses that influence crucial ecological processes, such as predator-prey interactions.

Sex-specific effects of inbreeding on body colouration and physiological colour change in the cichlid fish Pelvicachromis taeniatus.

BACKGROUND: Colour expression is highly variable in animals. In fishes, rapid colour change, i.e. physiological colour change, can be observed in multiple contexts, e.g. in camouflage or communication, and is affected by various factors, such as stress. Pelvicachromis taeniatus is a cichlid fish from West Africa with sexual dichromatism and both sexes being brightly coloured and flexible in ornament expression. In the present study, inbred and outbred P. taeniatus were photographed before and after a stress situation to investigate the stress response regarding colour expression in both sexes. RESULTS: The chromaticity and the colour patch size (relative coloured area at the abdomen) were determined at both timepoints and the changes were analysed. Additionally, the coefficients of variation within family groups for the chromaticity (CVchromaticity) and colour patch size (CVarea) were calculated. Chromaticity as well as the extent of colouration increased significantly following handling stress. The change in chromaticity was not significantly different between in- and outbred individuals in females and males. Inbred males showed more intense yellow colouration than outbred males. Independent from inbreeding, the CVchromaticity decreased following the handling stress. The change in CVarea of females and males differed between in- and outbred individuals. In females, the decrease was significantly stronger in inbred individuals and in males the decrease was stronger in the outbred group. CONCLUSION: The results show that short-term stress can increase colouration, potentially advertising individual's stress tolerance. Furthermore, this study shows positive inbreeding effects on a sexually selected trait.

Body coloration as a dynamic signal during intrasexual communication in a cichlid fish.

BACKGROUND: Intrasexual competition over access to resources can lead to aggression between individuals. Because overt aggression, i.e. fights, can be costly for contestants, the communication of aggressive motivation prior to engagement in a physical fight is often mediated by conventional signals. Animals of various taxa, including fishes, display visual signals such as body coloration that can dynamically be adjusted depending on the individual's motivation. Male individuals of the West African cichlid Pelvicachromis taeniatus express a yellow body coloration displayed during courtship but also in an intrasexual competition context. RESULTS: Within-individual variation in male yellow body coloration, as quantified with standardized digital photography and representation in a CIELab color space, was examined in a mating context by exposing males to a female and in a competitive intrasexual context, i.e. in a dyadic contest. Additionally, spectrometric reflectance measurements were taken to obtain color representations in a physiological color space based on spectral sensitivities of our model species. Exposure to females did not significantly affect male color expression. However, analysis of body coloration revealed a change in within-individual color intensity and colored area after interaction with a male competitor. In dominant males, extension of coloration was positively correlated with restrained aggression, i.e. displays, which in turn explained dominance established between the two contestants. CONCLUSION: Body coloration in male P. taeniatus is a dynamic signal that is used in concert with display behavior in communication during intrasexual competition.

Influence of lighting environment on social preferences in sticklebacks from two different photic habitats. II. Shoaling and mate preferences of lab-bred fishes.

Different environmental conditions may lead to diverse morphological, behavioral, and physiological adaptations of different populations of the same species. Lighting conditions, for example, vary vastly especially between aquatic habitats, and have been shown to elicit adaptations. The availability of short-wave ultraviolet (UV) light is especially fluctuating, as UV wavelengths are attenuated strongly depending on water properties. The island of North Uist, Scotland, comprises 2 differential habitat types, tea-stained and clear-water lakes, varying considerably in UV transmission. In previous studies, wild-caught 3-spined stickleback Gasterosteus aculeatus populations (3 populations of each habitat type) were tested with respect to their shoaling and mate preferences for fish viewed under UV-present and UV-absent conditions. The results revealed a habitat-dependent preference of UV cues during shoal choice (tea-stained populations: preference for UV-absent condition in tea-stained water; clear-water populations: no preference in clear-water) but an overall preference for UV-present conditions during mate choice. To assess genetic influences on these behavioral patterns, similar experiments were conducted with lab-bred F1-generations of the same stickleback populations that were raised in a common environment (i.e. standardized clear-water conditions). Offspring of sticklebacks from tea-stained lakes tended to prefer shoals viewed under UV-absent conditions (only in tea-stained water), while sticklebacks from clear-water lakes showed a significant preference for the shoal viewed under UV-present conditions in clear-water but not in tea-stained water. Mate-preference experiments demonstrated that females from the tea-stained lakes significantly preferred and females from the clear-water lakes preferred by trend the male viewed under UV-present conditions in the clear-water treatment. The results for both shoaling- and mate-preference tests were largely similar for wild-caught and lab-bred sticklebacks, thus hinting at a genetic basis for the preference patterns.

Intrasexual selection: Kin competition increases male-male territorial aggression in a monogamous cichlid fish.

During intrasexual competition, individuals of the same sex compete for access to breeding sites and mating partners, often accompanied by aggressive behavior. Kin selection theory predicts different kin-directed social interactions ranging from cooperation to aggression depending on the context and the resource in question. Kin competition reducing indirect fitness might be avoided by actively expelling relatives from territories and by showing higher aggression against kin. The West-African cichlid Pelvicachromis taeniatus is a monogamous cave breeder with males occupying and defending breeding sites against rivals. This species is capable of kin recognition and shows kin-preference during juvenile shoaling and mate choice. However, subadults of P. taeniatus seem to avoid the proximity of same-sex kin. In the present study, we examined territorial aggression of territory holders against intruding related and unrelated males as well as intruder's behavior. We observed higher aggression among related competitors suggesting that related males are less tolerated as neighbors. Avoidance of intrasexual competition with relatives might increase indirect fitness of males in monogamous species.

Differential investment in pre- and post-mating male sexual traits in response to prolonged exposure to ambient UVB radiation in a fish.

Increasing UVB radiation (UVB) reaching earth's surface following stratospheric ozone depletion is linked to serious consequences for organisms. While studies have focused on direct cytocidal and immunomodulatory effects of UVB, indirect consequences for fitness-related life-history traits are largely unexplored, although knowledge is needed to understand organismal responses to climate change. The present study investigates the effects of developmental exposure to enhanced, but ecologically relevant, ambient UVB levels on growth (body size), parental behavior (nest-building), fitness-enhancing traits of pre-mating (sexual ornamentation) and post-mating (sperm traits) sexual selection as well as their interrelationships in male three-spined sticklebacks (Gasterosteus aculeatus). Moreover, potentially underlying direct UVB effects, testicular antioxidant capacity (TAC) and testes and skin melanization were quantified. Juvenile full-siblings were split into two groups and raised until adulthood in a semi-natural set-up under light conditions including either natural (UVBnormal) or elevated UVB levels (UVBenhanced). When becoming reproductive, males were kept individually before data collection took place at their reproductive peak. The results showed that males from the UVBenhanced-group were smaller than their brothers from the UVBnormal-treatment, whereas no treatment differences were observed for sexual ornamentation, sperm traits and TAC. Moreover, UVB-stressed males built their nests faster and the relationship between body size and nest size was negative for UVBenhanced-males while being positive for UVBnormal-males. These results demonstrate that, depending on physical state, UVB-stressed males adjusted their behavior to some extent. Additionally, a trade-off between the investment in pre- and post-mating traits was found for UVBenhanced-males, i.e. the intensity of their breeding coloration was negatively correlated with sperm number whereas this relationship was reversed for UVBnormal-males, thus showing an interaction between pre- and post-mating traits regarding exposure treatment. The interaction provides first experimental evidence that differential allocation to energetically demanding pre- and post-mating components of male fitness is triggered by a key environmental stressor of climate change.