Teaching laboratory for large cohorts of undergraduates: Private and social information in fish.

A challenge in the Bachelor's studies in Biology is to strike a balance between reducing the teaching of practical scientific experiments to what is feasible in a short time, and teaching "real" science in undergraduate laboratories for high numbers of participants. We describe a laboratory in behavioral biology, with the primary focus on the student learning. However, also the underlying scientific question and the results of the experiment, namely the behavior of the three-spined stickleback (Gasterosteus aculeatus) in a trade-off situation during foraging, is without a doubt timely and sufficient for scientific studies on this subject, and this through the experiments conducted and data collected by the students. The students rated this laboratory well and learned at the end that social information is certainly important, but that self-learning can be more important, and this not only in small fish, but also for the students themselves.

Male and female preferences for nest characteristics under paternal care.

Nests play a critical role for offspring development across the animal kingdom. Nest quality may contribute to the builder's extended phenotype and serve as an ornament during mate choice. We examined male and female nest choice in the common goby (Pomatoschistus microps), a benthic fish with male-only parental care where females deposit eggs in male-built nests. Using prebuilt nest models, we independently manipulated two candidate nest quality traits: (a) nest entrance width with a role in oxygen ventilation, and (b) extent of sand cover with a role in camouflage. In simultaneous choice trials, male gobies exhibited no preference for any nest model type. This suggests that initial characteristics of a nesting substrate have minor importance for males, which usually remodel the nest. Females were given a choice between two males occupying either entrance- or cover-manipulated nests. The same pair of males was then exposed to a second female but now with alternated nest types assigned. Most females were consistent in choosing the same, typically the heavier male of the two regardless of nest properties. However, the females that chose the same nest regardless of the male preferred low over high sand coverage and narrow over wide nest entrance. Our results indicate that females base their mating decision on a combination of male phenotype and nest traits. While we found no indication that females are attracted to highly decorated nests, our study is the first in fishes to disentangle a preference for narrow (and thus more protective) nest entrances independent of nest coverage.

Ecological variation along the salinity gradient in the Baltic Sea Area and its consequences for reproduction in the common goby.

Although it has become clear that sexual selection may shape mating systems and drive speciation, the potential constraints of environmental factors on processes and outcomes of sexual selection are largely unexplored. Here, we investigate the geographic variation of such environmental factors, more precisely the quality and quantity of nest resources (bivalve shells) along a salinity gradient in the Baltic Sea Area (Baltic Sea, Sounds and Belts, and Kattegat). We further test whether we find any salinity-associated morphological differences in body size between populations of common gobies Pomatoschistus microps, a small marine fish with a resource-based mating system. In a geographically expansive field study, we sampled 5 populations of P. microps occurring along the salinity gradient (decreasing from West to East) in the Baltic Sea Area over 3 consecutive years. Nest resource quantity and quality decreased from West to East, and a correlation between mussel size and male body size was detected. Population density, sex ratios, mating- and reproductive success as well as brood characteristics also differed between populations but with a less clear relation to salinity. With this field study we shed light on geographic variation of distinct environmental parameters possibly acting on population differentiation. We provide insights on relevant ecological variation, and draw attention to its importance in the framework of context-dependent plasticity of sexual selection.

Female mating competition alters female mating preferences in common gobies.

Mating decisions can be affected by intrasexual competition and sensitive to operational sex-ratio (OSR) changes in the population. Conceptually, it is assumed that both male and female mate-competition may interfere with female reproductive decisions. Experimentally, however, the focus has been on the effect of male competition on mate choice. In many species with paternal care as in the common goby Pomatoschistus microps, the OSR is often female-biased and female mate-competition for access to available nesting males occurs. Using the same protocol for 3 experiments testing the effect of a perceived risk of female mate-competition, I studied female preferences for nest-holding males differing in its nest size (large/small), body size (large/small), and nest status (with/without eggs already in nest) and measured mating decisions, spawning latencies, and clutch size. Regardless of the social context, females preferred males with larger nests. A preference for large males was only expressed in presence of additional females. For nest status, there was a tendency for females to prefer mating with males with an empty nest. Here, female-female competition increased the propensity to mate. The results of this study show that females are sensitive to a female competitive social environment and suggest that in choice situations, females respond to the social context mainly by mating decisions per se rather than by adjusting the clutch size or spawning latency. Females base their mating decisions not only on a male's nest size but also on male size as an additional cue of mate quality in the presence of additional females.

Noise can affect acoustic communication and subsequent spawning success in fish.

There are substantial concerns that increasing levels of anthropogenic noise in the oceans may impact aquatic animals. Noise can affect animals physically, physiologically and behaviourally, but one of the most obvious effects is interference with acoustic communication. Acoustic communication often plays a crucial role in reproductive interactions and over 800 species of fish have been found to communicate acoustically. There is very little data on whether noise affects reproduction in aquatic animals, and none in relation to acoustic communication. In this study we tested the effect of continuous noise on courtship behaviour in two closely-related marine fishes: the two-spotted goby (Gobiusculus flavescens) and the painted goby (Pomatoschistus pictus) in aquarium experiments. Both species use visual and acoustic signals during courtship. In the two-spotted goby we used a repeated-measures design testing the same individuals in the noise and the control treatment, in alternating order. For the painted goby we allowed females to spawn, precluding a repeated-measures design, but permitting a test of the effect of noise on female spawning decisions. Males of both species reduced acoustic courtship, but only painted gobies also showed less visual courtship in the noise treatment compared to the control. Female painted gobies were less likely to spawn in the noise treatment. Thus, our results provide experimental evidence for negative effects of noise on acoustic communication and spawning success. Spawning is a crucial component of reproduction. Therefore, even though laboratory results should not be extrapolated directly to field populations, our results suggest that reproductive success may be sensitive to noise pollution, potentially reducing fitness.

You eat what you are: personality-dependent filial cannibalism in a fish with paternal care.

Many animal parents invest heavily to ensure offspring survival, yet some eventually consume some or all of their very own young. This so-called filial cannibalism is known from a wide range of taxa, but its adaptive benefit remains largely unclear. The extent to which parents cannibalize their broods varies substantially not only between species, but also between individuals, indicating that intrinsic behavioral differences, or animal personalities, might constitute a relevant proximate trigger for filial cannibalism. Using a marine fish with extensive paternal care, the common goby (Pomatoschistus microps), we investigated the influence of animal personality on filial cannibalism by assessing (1) behavioral consistency across a breeding and a nonbreeding context; (2) correlations between different breeding (egg fanning; filial cannibalism) and nonbreeding (activity) behaviors, and, in a separate experiment; (3) whether previously established personality scores affect filial cannibalism levels. We found consistent individual differences in activity across contexts. Partial filial cannibalism was independent of egg fanning but correlated strongly with activity, where active males cannibalized more eggs than less active males. This pattern was strong initially but vanished as the breeding season progressed. The incidence of whole clutch filial cannibalism increased with activity and clutch size. Our findings indicate that filial cannibalism cannot generally be adjusted independently of male personality and is thus phenotypically less plastic than typically assumed. The present work stresses the multidimensional interaction between animal personality, individual plasticity and the environment in shaping filial cannibalism.

Water mold infection but not paternity induces selective filial cannibalism in a goby.

Many animals heavily invest in parental care but still reject at least some of their offspring. Although seemingly paradoxical, selection can favor parents to neglect offspring of particularly low reproductive value, for example, because of small survival chances. We here assess whether filial cannibalism (FC), where parents routinely eat some of their own young, is selective in response to individual offspring reproductive value. We performed two independent laboratory experiments in the common goby (Pomatoschistus microps) to test whether caring fathers preferentially cannibalize eggs of a given infection history and paternity. While males did not discriminate kin from nonkin eggs, they consumed significantly more eggs previously exposed to water mold compared to uninfected eggs. Our findings clearly show that parents differentiate between eggs based on differences in egg condition, and thus complement the prevailing view that FC arises for energetic reasons. By preventing the spread of microbial infections, the removal of molded eggs can constitute an important component of parental care and may represent a key driver of selective FC in a wide array of parental fish.

Evolutionary and ecological implications of sexual parasitism.

Sexual parasites offer unique insights into asexual and sexual reproduction. They mate with a 'host' whose genetic contribution is discarded either immediately (in androgenesis or gynogenesis) or after a delay of one generation (in hybridogenesis). The discarded genome can be maternal or paternal, implying that not only females but also males can reproduce asexually. The resulting lineages are often older than ecological or evolutionary theory predicts. Sexual parasites have links to a diverse set of concepts: selfish genetic elements, degradation of clonal genomes, evolution of sex, mate-choice theory, and host-parasite dynamics. We discuss the different sexually parasitic systems in both hermaphrodites and gonochoristic organisms, emphasizing their similarities and differences in ecological and evolutionary settings.

Condition-dependence, genotype-by-environment interactions and the lek paradox.

The lek paradox states that maintaining genetic variation necessary for 'indirect benefit' models of female choice is difficult, and two interrelated solutions have been proposed. 'Genic capture' assumes condition-dependence of sexual traits, while genotype-by-environment interactions (GEIs) offer an additional way to maintain diversity. However, condition-dependence, particularly with GEIs, implies that environmental variation can blur the relationship between male displays and offspring fitness. These issues have been treated separately in the past. Here we combine them in a population genetic model, and show that predictions change not only in magnitude but also in direction when the timing of dispersal between environments relative to the life cycle is changed. GEIs can dramatically improve the evolution of costly female preferences, but also hamper it if much dispersal occurs between the life history stage where condition is determined and mating. This situation also arises if selection or mutation rates are too high. In general, our results highlight that when evaluating any mechanism promoted as a potential resolution of the lek paradox, it is not sufficient to focus on its effects on genetic variation. It also has to be assessed to what extent the proposed mechanism blurs the association between male attractiveness and offspring fitness; the net balance of these two effects can be positive or negative, and often strongly context-dependent.

Females increase current reproductive effort when future access to males is uncertain.

Trade-offs between current and future reproduction shape life histories of organisms, e.g. increased mortality selects for earlier reproductive effort, and mate limitation has been shown to shape male life histories. Here, we show that female life histories respond adaptively to mate limitation. Female common gobies (Pomatoschistus microps) respond to a female-biased operational sex ratio by strongly increasing the size of their first clutch. The plastic response is predicted by a model that assumes that females use the current competitive situation to predict future difficulties of securing a mating. Because female clutch size decisions are much more closely linked to population dynamics than male life-history traits, plastic responses to mate-finding limitations may be an underappreciated force in population dynamics.

How populations persist when asexuality requires sex: the spatial dynamics of coping with sperm parasites.

The twofold cost of sex implies that sexual and asexual reproduction do not coexist easily. Asexual forms tend to outcompete sexuals but may eventually suffer higher extinction rates, creating tension between short- and long-term advantages of different reproductive modes. The 'short-sightedness' of asexual reproduction takes a particularly intriguing form in gynogenetic species complexes, in which an asexual species requires sperm from a related sexual host species to trigger embryogenesis. Asexuals are then predicted to outcompete their host, after which neither species can persist. We examine whether spatial structure can explain continued coexistence of the species complex, and assess the evidence based on data on the Amazon molly (Poecilia formosa). A modification of the Levins metapopulation model creates two regions of good prospects for coexistence, connected by a region of poorer patch occupancy levels. In the first case, mate discrimination and/or niche differentiation keep local extinction rates low, and most patches contain both species; the other possibility resembles host-parasite dynamics where parasites frequently drive the host locally extinct. Several dynamical features are counterintuitive and relate to the parasitic nature of interactions in the species complex: for example, high local extinction rates of the asexual species can be beneficial for its own persistence. This creates a link from the evolution of sexual reproduction to that of prudent predation.

Condition-dependence, genotype-by-environment interactions and the lek paradox.

The lek paradox states that maintaining genetic variation necessary for 'indirect benefit' models of female choice is difficult, and two interrelated solutions have been proposed. 'Genic capture' assumes condition-dependence of sexual traits, while genotype-by-environment interactions (GEIs) offer an additional way to maintain diversity. However, condition-dependence, particularly with GEIs, implies that environmental variation can blur the relationship between male displays and offspring fitness. These issues have been treated separately in the past. Here we combine them in a population genetic model, and show that predictions change not only in magnitude but also in direction when the timing of dispersal between environments relative to the life cycle is changed. GEIs can dramatically improve the evolution of costly female preferences, but also hamper it if much dispersal occurs between the life history stage where condition is determined and mating. This situation also arises if selection or mutation rates are too high. In general, our results highlight that when evaluating any mechanism promoted as a potential resolution of the lek paradox, it is not sufficient to focus on its effects on genetic variation. It also has to be assessed to what extent the proposed mechanism blurs the association between male attractiveness and offspring fitness; the net balance of these two effects can be positive or negative, and often strongly context-dependent.

Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters.

Most eucaryotic organisms classified as living in an extreme habitat are invertebrates. Here we report of a fish living in a Mexican cave (Cueva del Azufre) that is rich in highly toxic H(2)S. We compared the water chemistry and fish communities of the cave and several nearby surface streams. Our study revealed high concentrations of H(2)S in the cave and its outflow (El Azufre). The concentrations of H(2)S reach more than 300 muM inside the cave, which are acutely toxic for most fishes. In both sulfidic habitats, the diversity of fishes was heavily reduced, and Poecilia mexicana was the dominant species indicating that the presence of H(2)S has an all-or-none effect, permitting only few species to survive in sulfidic habitats. Compared to habitats without H(2)S, P. mexicana from the cave and the outflow have a significantly lower body condition. Although there are microhabitats with varying concentrations of H(2)S within the cave, we could not find a higher fish density in areas with lower concentrations of H(2)S. We discuss that P. mexicana is one of the few extremophile vertebrates. Our study supports the idea that extreme habitats lead to an impoverished species diversity.

Choosy males from the underground: male mating preferences in surface- and cave-dwelling Atlantic mollies (Poecilia mexicana).

Atlantic mollies (Poecilia mexicana) inhabit a variety of surface habitats, but they also occur in a sulfur cave in southern Mexico. We examined male mate choice relative to female body size in the cave population and in the most closely related surface-dwelling population from a nearby river. Males from both populations were either light- or dark-reared and could choose between two differently sized females either on the basis of visual cues in light or on the basis of solely nonvisual cues in darkness. Sexual preferences were estimated from the degree of association. Cave molly males always showed a preference for the larger female, both in light and in darkness. Among the surface males, only light-reared males showed a preference in the visual cues test, but not in darkness. In a control experiment, we demonstrated that male association preferences directly translate into actual mating preferences. Apparently, using visual cues for mate choice is the ancestral state in this system, and using nonvisual cues has evolved as a novel trait in the cave population. We discuss the evolution of nonvisual male mate choice in the context of changed environmental conditions, namely the absence of light, hypoxia, and toxic hydrogen sulfide in the cave.