Patterns of multiple paternity and maternity in fishes

The characterization of patterns of multiple mating is a major facet of molecular ecology and is paramount to understanding the evolution of behaviours associated with parental care and mate choice. Over the last 15 years, fishes have been particularly well studied with respect to multiple maternity and paternity thanks to the widespread application of microsatellite markers. The present review focusses on the impressive literature on genetic parentage in fishes. In studies of natural populations, we find that multiple paternity is extremely common across fish species, whereas rates of multiple maternity are much more variable. In species with nest defence, for example, rates of multiple maternity are strongly bimodal, and the occurrence of multiple dams per brood is either rare or the rule. The sex of the care‐giving parent is correlated with the rate of multiple parentage: when males provide uniparental care, rates of multiple paternity are low compared to rates of multiple maternity; when females provide parental care, either alone or assisted by males, rates of multiple paternity are highly variable, whereas rates of multiple maternity are quite low. These patterns may reflect conflicts between the reproductive interests of males and females. We also find that fishes in which females brood the offspring internally display much higher rates of multiple paternity compared to mammals or birds, whereas reptiles are intermediate. Male‐nesting fish species, however, show rates of multiple paternity more similar to those found in other vertebrates. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 735–760.     

Animal breeding systems

The study of breeding systems explores relationships between mating behaviour and parental care. Recent findings have shown that in many birds, fishes, anurans, and insects, females play a more active role than previously thought, by engaging in mate choice, mating with more than one male, and selecting genetic partners separately from social partners. Theoretical advances have improved our understanding of the effect of parental care on sex differences in mating behaviour, though less attention has been devoted to feedback in the opposite direction. The original emphasis on the role of ecology in determining breeding systems has been overshadowed by studies of individual interactions, but modern comparative techniques may provide a new fusion between ecology, life histories, and reproductive behaviour.     

Do Male Desert Gobies Compromise Offspring Care to Attract Additional Mating Opportunities?

Males often play a critical role in offspring care but the time and energy invested in looking after young can potentially limit their ability to seek out additional mating opportunities. Recent studies, however, suggest that a conflict between male parental effort and mating effort may not always be inevitable, especially if breeding occurs near the nest, or if parental behaviours are under sexual selection. Accordingly, we set out to experimentally investigate male care and courtship in the desert goby Chlamydogobius eremius, a nest-guarding fish with exclusive paternal care. Despite courtship occurring near the nest, we found that when egg-tending males were given the opportunity to attract additional females, they fanned their eggs less often, engaged in shorter fanning bouts, and spent more of their time outside their nests courting. Our findings highlight the importance of understanding the circumstances under which reproductive tradeoffs are expected to occur and how these, in turn, operate to influence male reproductive decisions.     

Genetic perspectives on the natural history of fish mating systems

Molecular analyses of bird and mammal populations have shown that social mating systems must be distinguished from genetic mating systems. This distinction is important in fishes also, where the potential for extrapair spawning and intraspecific brood parasitism is especially great. We review studies on fishes that have used molecular markers to document biological parentage and genetic mating systems in nature, particularly in species with extended parental care of offspring. On average, nest-guarding adults parented about 70-95% of their custodial offspring, and approximately one-third of the nests were cuckolded to some extent. Furthermore, nearly 10% of the assayed nests contained offspring tended by foster fathers either because of nest takeovers or egg thievery. On average, fish that provide parental care on nests spawned with more mates than did fish with internal fertilization and pregnancy. Overall, genetic markers have both confirmed and quantified the incidence of several reproductive and other social behaviors of fishes, and have thereby enhanced our knowledge of piscine natural history.     

Fishes as models in studies of sexual selection and parental care

Fishes are by far the most diverse group of vertebrates. This fact is in no way, however, reflected in their use as model organisms for understanding sexual selection or parental care. Why is this so? Is it because fishes are actually poor models? The usefulness of fishes as models for sexual selection and parental care is discussed by emphasizing some problems inherent in fish studies, along with a number of reasons why fishes are indeed excellently suited. The pros and cons of fishes as models are discussed mainly by comparison with birds, the most popular model organisms in animal behaviour. Difficulties include a lack of background knowledge for many species, and the problems of marking and observing fishes in their natural environment. Positive attributes include the diversity of lifestyles among fishes, and the ease with which they can be studied experimentally in the laboratory. How useful fish models can be is briefly illustrated by the impressive and broadly relevant advances derived from studies of guppies Poecilia reticulata and three‐spined sticklebacks Gasterosteus aculeatus . A selection of topics is highlighted where fish studies have either advanced or could greatly enhance, the understanding of processes fundamental to animal reproductive dynamics. Such topics include sex role dynamics, the evolution of female ornamentation and mate choice copying. Finally, a number of potential pitfalls in the future use of fish as models for sexual selection and parental care are discussed. Researchers interested in these issues are recommended to make much more extensive use of fish models, but also to adopt a wider range of models among fishes.     

Genetic monogamy despite social promiscuity in the pot-bellied seahorse (Hippocampus abdominalis)

Sexual selection theory predicts a positive correlation between relative parental investment and mate choice. In syngnathid fishes (seahorses and pipefish), males brood offspring in specialized brooding structures. While female-female mating competition has been demonstrated in some pipefishes, all seahorses (genus Hippocampus) studied to date have been found to have conventional sex roles with greater male-male competition for access to mates despite possessing the most complex brood structures in the family. Although multiple mating is common in pipefish, seahorses are again exceptional, exhibiting strict genetic monogamy. Both demographic and behavioural explanations have been offered to explain the lack of multiple mating in seahorse species, but these hypotheses have not yet been explicitly addressed. We investigated mating systems and brood parentage of the pot-bellied seahorse, Hippocampus abdominalis, a temperate-water species that is socially promiscuous with conventional sex roles in laboratory populations. We observed promiscuous courtship behaviour and sex-role reversal in high density, female-biased field populations of H. abdominalis. We hypothesize that sex roles are plastic in H. abdominalis, depending on local population density and sex ratio. Despite promiscuous courtship behaviour, all assayed male seahorses were genetically monogamous in both laboratory and wild populations. Physiological limitations associated with embryo incubation may explain the absence of multiple mating in seahorses and may have played an important role in the development of the unique reproductive behaviour typical in these species.     

Sperm competition,sexual selection and the diverse reproductive biology of Osteoglossiformes

Osteoglossiformes are an order of “bony tongue” fish considered the most primitive living order of teleosts. This review seeks to consolidate known hypotheses and identify gaps in the literature regarding the adaptive significance of diverse reproductive traits and behaviour of osteoglossiforms within the context of sperm competition and the wider lens of sexual selection. Many of the unusual traits observed in osteoglossiforms indicate low levels of sperm competition; most species have unpaired gonads, and mormyroids are the only known vertebrate species with aflagellate sperm. Several osteoglossiform families have reproductive anatomy associated with internal fertilization but perform external fertilization, which may be representative of the evolutionary transition from external to internal fertilization and putative trade-offs between sperm competition and the environment. They also employ every type of parental care seen in vertebrates. Geographically widespread and basally situated within teleosts, osteoglossiforms present an effective study system for understanding how sperm competition and sexual selection have shaped the evolution of teleost reproductive behaviour, sperm and gonad morphology, fertilization strategies, courtship and paternal care, and sexual conflict. The authors suggest that the patterns seen in osteoglossiform reproduction are a microcosm of teleost reproductive diversity, potentially signifying the genetic plasticity that contributed to the adaptive radiation of teleost fishes.     

Nesting, courtship and kidney hypertrophy in Schistocephalus-infected male three-spined stickleback from an upland lake

The effect of Schistocephalus solidus infection on reproductive development and behaviour of male three-spined stickleback Gasterosteus aculeatus from an upland lake (Llyn Frongoch, Wales, U.K.) was investigated. Uninfected and infected males were collected on two separate occasions during the 2005 breeding season and encouraged to build nests under favourable laboratory conditions. Male nuptial colouration, courtship levels and nesting activity were recorded daily over two separate 21 day studies. Completed nests were removed, encouraging males to build multiple nests. On termination of each study, males were dissected and the kidney and any S. solidus plerocercoids were removed and weighed. In contrast to uninfected males, which readily built multiple nests, no infected males completed a nest during either study. Infected males also exhibited significantly reduced courtship levels, nesting activity, nuptial colouration, kidney development and body condition, compared with uninfected fish. Among infected three-spined stickleback, courtship and nesting behaviours tended to be more severely impacted in fish harbouring heavier plerocercoid burdens. In contrast to other populations, male three-spined stickleback from Llyn Frongoch appear to be unable to overcome the negative impacts of infections on reproductive development and behaviour when provided with short-term favourable conditions. Discrepancies between populations might have been related to the trophic status at the site of capture, emphasizing the importance of studying the biological effects of infections under different environmental conditions.     

Culture and courtship in vertebrates: a review of social learning and transmission of courtship systems and mating patterns

Female and male animals often choose mates based upon the complementarity of their courtship behaviours and preferences. The importance of this fact on the evolutionary dynamics of populations has long been appreciated. What has not been appreciated is the role that social learning might play in the transmission of systems of courtship behaviour across generations. This paper addresses the social transmission of courtship behavioural traditions in vertebrates. It discusses views of culture in the context of behavioural signals and preferences in courtship. It then reviews empirical evidence for culture-like processes affecting courtship behaviour, focusing on studies of song learning in passerine birds and work on social learning of mating preferences. The paper concludes with potential future directions for research on social traditions in systems of courtship behaviour, including determining mechanisms of transmission, genetic and non-social environmental effects, and selective factors influencing the stability of behavioural traditions over time. By integrating proximate and ultimate questions for the transmission of courtship systems, this work would increase our understanding of the ways individual development, cultural processes, and population evolution influence, and are in turn influenced by, one another.     

Effects of parasites on fish behaviour: a review and evolutionary perspective

Fish serve as hosts to a range of parasites that are taxonomically diverse and that exhibit a wide variety of life cycle strategies. Whereas many of these parasites are passed directly between ultimate hosts, others need to navigate through a series of intermediate hosts before reaching a host in (or on) which they can attain sexual maturity. The realisation that parasites need not have evolved to minimise their impact on hosts to be successful, and in many cases may even have a requirement for their hosts to be eaten by specific predators to ensure transmission, has renewed interest in the evolutionary basis of infection-associated host behaviour. Fishes have proved popular models for the experimental examination of such hypotheses, and parasitic infections have been demonstrated to have consequences for almost every aspect of fish behaviour. Despite a scarcity of knowledge regarding the mechanistic basis of such behaviour changes in most cases, and an even lower understanding of their ecological consequences, there can be little doubt that infection-associated behaviour changes have the potential to impact severely on the ecology of infected fishes. Changes in foraging efficiency, time budget, habitat selection, competitive ability, predator-prey relationships, swimming performance and sexual behaviour and mate choice have all been associated with – and in some cases been shown to be a result of – parasite infections, and are reviewed here in some detail. Since the behavioural consequences of infections are exposed to evolutionary selection pressures in the same way as are other phenotypic traits, few behavioural changes will be evolutionarily neutral and host behaviour changes that facilitate transmission should be expected. Despite this expectation, we have found little conclusive evidence for the Parasite Increased Trophic Transmission (PITT) hypothesis in fishes, though recent studies suggest it is likely to be an important mechanism. Additionally, since the fitness consequences of the many behavioural changes described have rarely been quantified, their evolutionary and ecological significance is effectively unknown.Potential hosts may also change their behaviour in the presence of infective parasite stages, if they adopt tactics to reduce exposure risk. Such `behavioural resistance', which may take the form of habitat avoidance, prey selectivity or avoidance of infected individuals, can be viewed as behavioural change associated with the threat of being parasitised, and so is included here. Actually harbouring infections may also stimulate fishes to perform certain types of simple or complex behaviours aimed at removing parasites, such as substrate scraping or the visitation of cleaning stations, although the efficacy of the latter as a parasite removal strategy is currently subject to a good deal of debate.The effects parasites have on shoaling behaviour of host fish have attracted a good deal of attention from researchers, and we have provided a case study to summarise the current state of knowledge. Parasites have been shown to affect most of the antipredator effects of shoaling (such as vigilance, co-ordinated evasion and predator confusion) and can also impair an individual's foraging ability. It therefore seems unsurprising that, in a number of species avoidance of parasitised individuals has evolved which may explain the occurrence of parasite-assorted shoals in the field. Parasitised fish are found more often in peripheral shoal positions and show a reduced tendency for shoaling in some fish species. Given the array of host behaviours that may be changed, the fitness consequences of shoal membership for parasitised hosts and their parasites are not always easy to predict, yet an understanding of these is important before we can make predictions regarding the ecological impact of infections on host fish populations.Clearly, there remain many gaps in our knowledge regarding the effects of parasites on the behaviour of host fish. We believe that a much greater understanding of the importance of infection-associated behaviour changes in fish could be gained from high quality research in comparatively few areas. We have completed our review by highlighting the key research topics that we believe should attract new research in this field.     

Pheromonal inhibition of male courtship behaviour in the brown tree snake, Boiga irregularis: a mechanism for the rejection of potential mates

Pheromones play a central role in coordinating the events leading up to copulation in snakes. We report here a novel pheromone system in the brown tree snake in which females release a pheromone that inhibits male courtship behaviour. In a previous study, we made observations of female brown tree snakes releasing cloacal secretions (CS) during courtship that appeared to cause courting males to cease courtship. All snakes have glands that release CS through ducts located along the cloacal orifice. Although CS have been studied for many years, their function in the mediation of snake behaviour has not been experimentally well determined. We examined the role of CS in the reproductive behaviour of male and female brown tree snakes. We conducted four experiments to test the effect of both male and female CS on brown tree snake behaviour under two behavioural contexts, courtship and male-male ritualized combat. Within each experiment, we compared the effects of CS to a control. Female CS caused a decrease in the time that males spent courting females and a decrease in the intensity of courtship compared with the control treatment. Male CS did not, however, affect the time that males spent displaying courtship or the intensity of that courtship. Neither male nor female CS had significant effects on male ritualized combat behaviour, including time that males spent in combat or the intensity of combat behaviours displayed. Furthermore, neither female nor male CS had an effect on female courtship versus controls. The inhibition of brown tree snake reproductive behaviours is specific to female CS inhibiting male courtship behaviour. This pheromone acts in concert with the female sex pheromone to regulate the events leading to copulation.Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Sex steroid correlates of female-specific colouration,behaviour and reproductive state in Lake Eyre dragon lizards, <Emphasis Type="Italic">Ctenophorus maculosus</Emphasis>

In some species, females develop bright colouration to signal reproductive status and exhibit behavioural repertoires to incite male courtship and/or reduce male harassment and forced copulation. Sex steroids, including progesterone and testosterone, potentially mediate female reproductive colouration and reproductive behaviour. We measured associations among plasma profiles of testosterone and progesterone with variation in colour expression and reproductive behaviour, including unique courtship rejection behaviours, in female Lake Eyre dragon lizards, (Ctenophorus maculosus). At onset of breeding, progesterone and testosterone increased with vitellogenesis, coincident with colour intensification and sexual receptivity, indicated by acceptance of copulations. As steroid levels peaked around the inferred ovulation time, maximal colour development occurred and sexual receptivity declined. When females were gravid and exhibited maximal mate rejection behaviours, progesterone levels remained consistently high, while testosterone exhibited a discrete second peak. At oviposition, significant declines in plasma steroid levels, fading of colouration and a dramatic decrease in male rejection behaviours co-occurred. Our results indicate a generally concordant association among steroid levels, colouration, behaviour and reproductive events. However, the prolonged elevation in progesterone and a second peak of testosterone was unrelated to reproductive state or further colour change, possibly suggesting selection on females to retain high steroid levels for inducing rejection behaviours.     

Aggressive females become aggressive males in a sex-changing reef fish

Many animal populations display consistent individual differences in suites of correlated behaviours. While these so called 'animal personalities' can substantially influence the ecology and evolution of populations, little is known about cross-sex correlations of behaviour and thus the potential of personality to limit sex-specific behavioural adaptations. Here, we experimentally induced sex-change in the sequentially hermaphroditic reef fish Parapercis cylindrica and demonstrate the existence of tight cross-sex correlations for two behaviours with presumed different sex-specific optima. Individuals that were relatively more active and aggressive females were found to become relatively more active and aggressive males. By identifying personality as a potential genetic constraint on the resolution of intralocus sexual conflict over behaviour, our findings have important ecological and evolutionary implications for a wide range of species.     

The behaviour of Abudefduf zonatus (Pisces,pomacentridae) at Heron Island,Great Barrier Reef

Social organization and reproductive behaviour of Abudefduf zonatus were studied at Heron Island, Great Barrier Reef. This species is closely associated with the sand and coral substrate of the inner reef flat zone. Territorial, clustering, nest-digging, breeding and parental care behaviours are described. Mature males maintain territories for several weeks or longer around empty clam shells in which periodic spawning occurs. Females and sub-adult males hold territories interspersed among those of adult males. No pair bonds are formed, and eggs are guarded only by males. Breeding is roughly synchronized among fish of one area. Clustering behaviour may contribute to breeding syndrony in local populations.     

Antimicrobial egg cleaning by the fringed darter (Perciformes: Percidae: Etheostoma crossopterum): implications of a novel component of parental care in fishes

Broad-spectrum antimicrobial compounds have recently been identified in the epidermal mucus of fishes and probably serve as a first line of defence against microbial pathogens. Because of the ubiquitous nature of fungi and bacteria in aquatic systems, defence against these pathogens should be required throughout the lifespan of fishes, including the egg stage. We conducted experiments on Etheostoma crossopterum (Percidae: Catonotus), the fringed darter, to determine if the presence of a guarding male inhibits microbial colonization of eggs. Based on results from a combination of in-stream experiments, in vitro microbial assays, and morphological characteristics and behaviour of breeding males, we propose that antimicrobial egg cleaning by the guarding male is an effective component of parental care in these fish. Although innate antimicrobial compounds have been identified in a variety of organisms ranging from insects to vertebrates, integration of these compounds into a species's reproductive life history has been identified only in a small number of insect species. The results from this study not only indicate that E. crossopterum males provide a novel form of vertebrate parental care, but also have implications regarding the evolution of parental care in fishes and transitional evolutionary stages from no parental care to male parental care.     

Similarities in feeding behaviour between some marine and freshwater fishes in two tropical communities

The feeding behaviour and diets of fishes in two tropical habitats, a marine reef and a freshwater pond, were studied comparatively in Brazil. Similarities were found in the tactics employed to obtain food, the social patterns during foraging, and the general diet, notwithstanding lower-level taxonomic differences between the food items. The feeding behaviours of about one-third of the fish fauna from each community were approximately equivalent. The feeding categories of these fishes are briefly described. The similarities in the feeding modes probably reflect structural and functional properties shared by the two communities. Additional behavioural similarities of fishes in both habitats are presented and the lack of some particular foraging modes in each community is noted. The picture emerged that different, unrelated fish assemblages have the ability to evolve towards a similar behavioural and structural organization in response to comparable situations and constraints. The value of underwater observations and naturalistic studies on tropical freshwater fish assemblages is indicated.     

Reproductive potential of Schistocephalus solidus‐infected male three‐spined stickleback Gasterosteus aculeatus from two U.K. populations

Male three‐spined stickleback Gasterosteus aculeatus from two U.K. populations with endemic infections of the cestode Schistocephalus solidus were brought into the laboratory prior to the breeding season and transferred to nesting tanks under conditions designed to stimulate sexual maturation. Nesting and courtship behaviours were scored over a 35 day period, after which fish were euthanized and the liver, spleen, kidney and gonads were weighed. Among G. aculeatus from a park pond in Leicester, U.K., infected males rarely engaged in reproductive behaviours and exhibited reduced indices of sexual development, body condition and general health, with effects being largely independent of relative parasite mass (parasite index, I_P). In contrast, the reproductive behaviour of infected fish from Kendoon Loch in Dumfriesshire, U.K. appeared to be less severely affected, with infected fish regularly building nests and courting females under laboratory conditions. This was paralleled by a more limited effect of infection on physiological indicators of development, condition and general health. Furthermore, behavioural and physiological variables typically correlated with I_P among infected fish from this population. Although comparing the performance of infected fish from the two populations directly was difficult due to potentially confounding factors, the results support the findings of recent studies showing that the effects of S. solidus on host reproduction are unlikely to be uniform across G. aculeatus populations. One possibility is that variation in the effects of infection arises from differences in the co‐evolutionary association times of G. aculeatus with the parasite.