David Bierbach

EVOLUTION IN EXTREME ENVIRONMENTS: REPLICATED PHENOTYPIC DIFFERENTIATION IN LIVEBEARING FISH INHABITING SULFIDIC SPRINGS

We investigated replicated ecological speciation in the livebearing fish Poecilia mexicana and P. sulphuraria (Poeciliidae), which inhabit freshwater habitats and have also colonized multiple sulfidic springs in southern Mexico. These springs exhibit extreme hypoxia and high concentrations of hydrogen sulfide, which is lethal to most metazoans. We used phylogenetic analyses to test whether springs were independently colonized, performed phenotypic assessments of body and gill morphology variation to identify convergent patterns of trait differentiation, and conducted an eco‐toxicological experiment to detect differences in sulfide tolerances among ecotypes. Our results indicate that sulfidic springs were colonized by three different lineages, two within P. mexicana and one representing P. sulphuraria. Colonization occurred earlier in P. sulphuraria, whereas invasion of sulfidic springs in P. mexicana was more recent, such that each population is more closely related to neighboring populations from adjacent nonsulfidic habitats. Sulfide spring fish also show divergence from nonsulfidic phenotypes and a phenotypic convergence toward larger heads, larger gills, and increased tolerance to H2S. Together with previous studies that indicated significant reproductive isolation between fish from sulfidic and nonsulfidic habitats, this study provides evidence for repeated ecological speciation in the independent sulfide spring populations of P. mexicana and P. sulphuraria.

The evolutionary legacy of size-selective harvesting extends from genes to populations.

Size‐selective harvesting is assumed to alter life histories of exploited fish populations, thereby negatively affecting population productivity, recovery, and yield. However, demonstrating that fisheries‐induced phenotypic changes in the wild are at least partly genetically determined has proved notoriously difficult. Moreover, the population‐level consequences of fisheries‐induced evolution are still being controversially discussed. Using an experimental approach, we found that five generations of size‐selective harvesting altered the life histories and behavior, but not the metabolic rate, of wild‐origin zebrafish (Danio rerio). Fish adapted to high positively size selective fishing pressure invested more in reproduction, reached a smaller adult body size, and were less explorative and bold. Phenotypic changes seemed subtle but were accompanied by genetic changes in functional loci. Thus, our results provided unambiguous evidence for rapid, harvest‐induced phenotypic and evolutionary change when harvesting is intensive and size selective. According to a life‐history model, the observed life‐history changes elevated population growth rate in harvested conditions, but slowed population recovery under a simulated moratorium. Hence, the evolutionary legacy of size‐selective harvesting includes populations that are productive under exploited conditions, but selectively disadvantaged to cope with natural selection pressures that often favor large body size.

Genetic differentiation and selection against migrants in evolutionarily replicated extreme environments.

We investigated mechanisms of reproductive isolation in livebearing fishes (genus Poecilia) inhabiting sulfidic and nonsulfidic habitats in three replicate river drainages. Although sulfide spring fish convergently evolved divergent phenotypes, it was unclear if mechanisms of reproductive isolation also evolved convergently. Using microsatellites, we found strongly reduced gene flow between adjacent populations from different habitat types, suggesting that local adaptation to sulfidic habitats repeatedly caused the emergence of reproductive isolation. Reciprocal translocation experiments indicate strong selection against immigrants into sulfidic waters, but also variation among drainages in the strength of selection against immigrants into nonsulfidic waters. Mate choice experiments revealed the evolution of assortative mating preferences in females from nonsulfidic but not from sulfidic habitats. The inferred strength of sexual selection against immigrants (RIs) was negatively correlated with the strength of natural selection (RIm), a pattern that could be attributed to reinforcement, whereby natural selection strengthens behavioral isolation due to reduced hybrid fitness. Overall, reproductive isolation and genetic differentiation appear to be replicated and direct consequences of local adaptation to sulfide spring environments, but the relative contributions of different mechanisms of reproductive isolation vary across these evolutionarily independent replicates, highlighting both convergent and nonconvergent evolutionary trajectories of populations in each drainage.

Male fish use prior knowledge about rivals to adjust their mate choice

Mate choice as one element of sexual selection can be sensitive to public information from neighbouring individuals. Here, we demonstrate that males of the livebearing fish Poecilia mexicana gather complex social information when given a chance to familiarize themselves with rivals prior to mate choice. Focal males ceased to show mating preferences when being observed by a rival (which prevents rivals from copying mating decisions), but this effect was only seen when focal males have perceived rivals as sexually active. In addition, focal males that were observed by a familiar, sexually active rival showed a stronger behavioural response when rivals were larger and thus, more attractive to females. Our study illustrates an unparalleled adjustment in the expression of mating preferences based on social cues, and suggests that male fish are able to remember and strategically exploit information about rivals when performing mate choice.

RoboFish: increased acceptance of interactive robotic fish with realistic eyes and natural motion patterns by live Trinidadian guppies.

In recent years, simple biomimetic robots have been increasingly used in biological studies to investigate social behavior, for example collective movement. Nevertheless, a big challenge in developing biomimetic robots is the acceptance of the robotic agents by live animals. In this contribution, we describe our recent advances with regard to the acceptance of our biomimetic RoboFish by live Trinidadian guppies (Poecilia reticulata). We provide a detailed technical description of the RoboFish system and show the effect of different appearance, motion patterns and interaction modes on the acceptance of the artificial fish replica. Our results indicate that realistic eye dummies along with natural motion patterns significantly improve the acceptance level of the RoboFish. Through the interactive behaviors, our system can be adjusted to imitate different individual characteristics of live animals, which further increases the bandwidth of possible applications of our RoboFish for the study of animal behavior.

Sperm competition risk affects male mate choice copying

Mate choice copying was mostly described as a strategy employed by females to assess the quality of potential mates, but also males can copy other males’ mate choice. An open question in this context is whether and how copying males evaluate sperm competition risk, as mating with a female that has already copulated with another male obviously sets the stage for intense sperm competition (i.e., in species with internal fertilization). Using the livebearing Atlantic molly (Poecilia mexicana) as a model, we asked (a) whether males of that species indeed copy other males’ choices, and if they do so, (b) whether copying males strategically adjust their behavior to sperm competition risk. We used an approach where focal males could first choose to associate with a large or a small stimulus female. Mate choice tests were then repeated after an “observation phase” during which either no model male was present (treatment 1, control) or the previously non-preferred female could be seen associating (treatment 2) or physically interacting (treatment 3) with a model male. We found that, after the observation phase, males spent considerably more time with the previously non-preferred female in treatment (2), i.e., they copied the model male’s choice. This effect was much weaker during treatment (3) where sexual interactions between the model male and the formerly non-preferred female were allowed. Males, therefore, seem to adjust their copying behavior strategically to the perceived risk of sperm competition.

Divergent evolution of male aggressive behaviour: another reproductive isolation barrier in extremophile poeciliid fishes?

Reproductive isolation among locally adapted populations may arise when immigrants from foreign habitats are selected against via natural or (inter-)sexual selection (female mate choice). We asked whether also intrasexual selection through male-male competition could promote reproductive isolation among populations of poeciliid fishes that are locally adapted to extreme environmental conditions [i.e., darkness in caves and/or toxic hydrogen sulphide (H2S)]. We found strongly reduced aggressiveness in extremophile P. oecilia mexicana, and darkness was the best predictor for the evolutionary reduction of aggressiveness, especially when combined with presence of H2S. We demonstrate that reduced aggression directly translates into migrant males being inferior when paired with males from non-sulphidic surface habitats. By contrast, the phylogenetically old sulphur endemic P. sulphuraria from another sulphide spring area showed no overall reduced aggressiveness, possibly indicating evolved mechanisms to better cope with H2S.

Behavioural individuality in clonal fish arises despite near-identical rearing conditions

Behavioural individuality is thought to be caused by differences in genes and/or environmental conditions. Therefore, if these sources of variation are removed, individuals are predicted to develop similar phenotypes lacking repeatable individual variation. Moreover, even among genetically identical individuals, direct social interactions are predicted to be a powerful factor shaping the development of individuality. We use tightly controlled ontogenetic experiments with clonal fish, the Amazon molly (Poecilia formosa), to test whether near-identical rearing conditions and lack of social contact dampen individuality. In sharp contrast to our predictions, we find that (i) substantial individual variation in behaviour emerges among genetically identical individuals isolated directly after birth into highly standardized environments and (ii) increasing levels of social experience during ontogeny do not affect levels of individual behavioural variation. In contrast to the current research paradigm, which focuses on genes and/or environmental drivers, our findings suggest that individuality might be an inevitable and potentially unpredictable outcome of development.

Blending in with the Shoal: Robotic Fish Swarms for Investigating Strategies of Group Formation in Guppies

Robotic fish that dynamically interact with live fish shoals dramatically augment the toolset of behavioral biologists. We have developed a system of biomimetic fish for the investigation of collective behavior in Guppies and similarly small fish. This contribution presents full implementation details of the system and promising experimental results. Over long durations our robots are able to integrate themselves into shoals or recruit the group to exposed locations that are usually avoided. This system is the first open-source project for both software and hardware components and is supposed to facilitate research in the emerging field of bio-hybrid societies.

Homosexual behaviour increases male attractiveness to females

Male homosexual behaviour—although found in most extant clades across the Animal Kingdom—remains a conundrum, as same-sex mating should decrease male reproductive fitness. In most species, however, males that engage in same-sex sexual behaviour also mate with females, and in theory, same-sex mating could even increase male reproductive fitness if males improve their chances of future heterosexual mating. Females regularly use social information to choose a mate; e.g. male attractiveness increases after a male has interacted sexually with a female (mate choice copying). Here, we demonstrate that males of the tropical freshwater fish Poecilia mexicana increase their attractiveness to females not only by opposite-sex, but likewise, through same-sex interactions. Hence, direct benefits for males of exhibiting homosexual behaviour may help explain its occurrence and persistence in species in which females rely on mate choice copying as one component of mate quality assessment.