Katja U. Heubel

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.

Cave molly females (Poecilia mexicana, Poeciliidae, Teleostei) like well-fed males

We examined the preference of Atlantic molly females (Poecilia mexicana) to associate with a well-fed or a starved male in simultaneous choice tests. Females from three different populations were tested in three treatments: (1) the females could choose on the basis of multiple cues from the males (visual plus non-visual); (2) only non-visual cues could be perceived in darkness, (3) only visual cues were presented. The three tested populations differ clearly in their ecology: one population occurs in a typical river habitat, the second one in a milky sulfur creek outside a cave, and the third population occurs in a cave habitat (cave molly). In the river-dwelling population, females never showed a preference. In the population from the sulfur creek, females preferred to associate with the well-nourished male when visual cues from the males were available. Only cave molly females exhibited a strong preference for well-nourished males in all treatments. A morphological comparison demonstrated that wild-caught males from river habitats are typically in a good nutritional state. In the sulfur creek, males showed signs of starvation. Cave molly males were in an even worse nutritional state. In the cave population, saturated males probably indicate high fitness, thereby driving the evolution of the preference for good male nutritional state.

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.

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.

Geographic variation in female mate-copying in the species complex of a unisexual fish, Poecilia formosa

Summary The Amazon molly, Poecilia formosa, is a gynogenetic, all-female fish. Its mating system relies on heterospecific matings with males of closely related sexual species. In mixed populations, males mate with conspecific sexual females and heterospecific asexual females. Such matings are not isolated dyadic interactions but rather elements of a communication network, because multiple females can observe these interactions. This is the only known case of heterospecific mate-copying and, thus, a system in which the potential for mate-copying could be influenced by the presence of another species. Here we show that mate-copying is exhibited by the sexual species P. mexicana and P. latipinna, and the asexual P. formosa . Both sexual and asexual females copy each other’s mate choice decisions in sympatry, but females from allopatric populations do not show heterospecific mate-copying. Males benefit from heterospecific matings with Amazon mollies because these increase their attractiveness to the conspecific sexual females. In mixed shoals, mate-copying potentially imposes costs as it increases a male’s attractiveness to heterospecific females. We argue that the net-effect of mate-copying is beneficial to males because the relative strength of mate-copying is lower in Amazon mollies. We hypothesize that an added benefit to males lies in the signal value of copulations.

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.

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

Abstract 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

Abstract 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.

Old but gold: males preferentially cannibalize young eggs

Although counterintuitive at first sight, filial cannibalism is common in the animal kingdom and has been recognized as a mechanism to increase the cannibalizing parent’s lifetime reproductive success. However, previous evidence is often inconclusive and the adaptiveness of filial cannibalism is still not fully understood. We here address the notion that parents do not cannibalize at random but preferably consume offspring with a particular phenotype. To assess if differences in developmental stage and thus reproductive value of eggs trigger such selectivity, we experimentally presented male common gobies (Pomatoschistus microps) with two differently aged egg clutches within mixed broods. We found that males consumed significantly more young than old eggs. This result indicates that parents are not only able to discriminate between eggs based on developmental stage, but might use this to reduce the cost of partial filial cannibalism by selectively removing eggs of lower reproductive value.

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.