Social Environment Influences the Temporal Dynamics of Sneak-Spawning in a Fish with Alternative Reproductive Tactics.

AbstractSeveral predictions of sperm competition theory are not well supported empirically. One potential reason is that most current theory and empirical research ignore how the social environment influence the temporal dynamics of mating. We propose that understanding these dynamics is key to understanding sexual selection and improving the predictive power of theory. To demonstrate the importance of these dynamics, we quantify how males' social role, interactions among males, and current social environment influence the timing of mating in Symphodus ocellatus, a species with three alternative male reproductive tactics. Nesting males spawn synchronously with females; sneakers and satellites sneak-spawn with some time delay. Satellites also cooperate with nesting males. We found that satellites have shorter sneak-spawning delays than sneakers, a benefit of their cooperation with nesting males. Sneak-spawning delays decreased with increasing nest activity for sneakers but not for satellites, suggesting that sneakers may benefit from increased sperm competition intensity. Current sperm competition models ignore this potential benefit, which may be why the prediction that males should decrease investment when sperm competition involves more than two males is not well supported. Our study provides insight into mechanisms that drive variation in the timing of spawning, which could explain mismatches between theoretical and empirical results.

Experimentally induced variation in neuroendocrine processes affects male reproductive behaviour, sperm characteristics and social interactions.

While extensive research has focused on how social interactions evolve, the fitness consequences of the neuroendocrine mechanisms underlying these interactions have rarely been documented, especially in the wild. Here, we measure how the neuroendocrine mechanisms underlying male behaviour affect mating success and sperm competition in the ocellated wrasse (Symphodus ocellatus). In this species, males exhibit three alternative reproductive types. "Nesting males" provide parental care, defend territories and form cooperative associations with unrelated "satellites," who cheat by sneaking fertilizations but help by reducing sperm competition from "sneakers" who do not cooperate or provide care. To measure the fitness consequences of the mechanisms underlying these social interactions, we used "phenotypic engineering" that involved administering an androgen receptor antagonist (flutamide) to wild, free-living fish. Nesting males treated with flutamide shifted their aggression from sneakers to satellite males and experienced decreased submissiveness by sneaker males (which correlated with decreased nesting male mating success). The preoptic area (POA), a region controlling male reproductive behaviours, exhibited dramatic down-regulation of androgen receptor (AR) and vasotocin 1a receptor (V1aR) mRNA following experimental manipulation of androgen signalling. We did not find a direct effect of the manipulation on male mating success, paternity or larval production. However, variation in neuroendocrine mechanisms generated by the experimental manipulation was significantly correlated with changes in behaviour and mating success: V1aR expression was negatively correlated with satellite-directed aggression, and expression of its ligand arginine vasotocin (AVT) was positively correlated with courtship and mating success, thus revealing the potential for sexual selection on these mechanisms.

Intentional multiple mating by females in a species where sneak fertilization circumvents female choice for parental males.

This paper describes how individual female ocellated wrasse Symphodus ocellatus distribute their spawning among males and nests in space and time. It is based on previously collected genetic data of larvae from ten different nests (used to reconstruct half and full-sibling groupings both within and among nests on multiple days) and behavioural data of marked females across the reproductive season. Both the genetic analyses and behavioural observations confirm that female S. ocellatus intentionally engage in multiple mating, by repeatedly spawning at the same nest on different days and at several different nests (up to 12 spawning events over 3 weeks), leading to mixed paternity among her young. The main benefit of such high and intentional multiple mating is probably insurance against brood failure due to nest predation, desertion or poor paternal care by the male. These findings reveal that even in systems where females attempt to avoid male-controlled mixed paternity, they may still engage in intentional multiple mating due to these potential benefits.

Ocean acidification affects fish spawning but not paternity at CO2 seeps.

Fish exhibit impaired sensory function and altered behaviour at levels of ocean acidification expected to occur owing to anthropogenic carbon dioxide emissions during this century. We provide the first evidence of the effects of ocean acidification on reproductive behaviour of fish in the wild. Satellite and sneaker male ocellated wrasse (Symphodus ocellatus) compete to fertilize eggs guarded by dominant nesting males. Key mating behaviours such as dominant male courtship and nest defence did not differ between sites with ambient versus elevated CO2 concentrations. Dominant males did, however, experience significantly lower rates of pair spawning at elevated CO2 levels. Despite the higher risk of sperm competition found at elevated CO2, we also found a trend of lower satellite and sneaker male paternity at elevated CO2 Given the importance of fish for food security and ecosystem stability, this study highlights the need for targeted research into the effects of rising CO2 levels on patterns of reproduction in wild fish.

Does the risk of sperm competition help explain cooperation between reproductive competitors? A study in the ocellated wrasse (Symphodus ocellatus).

Although cooperating individuals may gain benefits, they risk being cheated by their allies. Therefore, to understand the persistence of cooperation by mutual benefits, it is important to document both the potential benefits of cooperation and the risks of cheating. We experimentally examined evidence of cooperation in the ocellated wrasse (Symphodus ocellatus), a fish species with males that exercise three reproductive strategies: satellite and sneaker males attempt to parasitically spawn in the nests of nesting males. Nesting males have been hypothesized to tolerate satellites as a result of satellite aid in defense against sneaker males and help in courting females. Here, we provide evidence that cooperation between reproductive competitors may arise in response to sperm competition from other males. After we experimentally removed satellites, nesting males had more sneakers at their nest and experienced a higher rate of sneaking when they spawned (increased sperm competition risk). When we experimentally distracted nesting males to prevent their acting aggressively toward satellites, satellites spawned with females and ate eggs in the nest. Our results suggest that nesting males and satellites gain fitness benefits of reduced direct reproductive and sperm competition through cooperation. However, nesting males risk losing paternity, while satellites experience increased aggression and must invest in aggression themselves (i.e., they act aggressively toward sneakers).

Female promiscuity promotes the evolution of faster sperm in cichlid fishes.

Sperm competition, the contest among ejaculates from rival males to fertilize ova of a female, is a common and powerful evolutionary force influencing ejaculate traits. During competitive interactions between ejaculates, longer and faster spermatozoa are expected to have an edge; however, to date, there has been mixed support for this key prediction from sperm competition theory. Here, we use the spectacular radiation of cichlid fishes from Lake Tanganyika to examine sperm characteristics in 29 closely related species. We provide phylogenetically robust evidence that species experiencing greater levels of sperm competition have faster-swimming sperm. We also show that sperm competition selects for increases in the number, size, and longevity of spermatozoa in the ejaculate of a male, and, contrary to expectations from theory, we find no evidence of trade-offs among sperm traits in an interspecific analysis. Also, sperm swimming speed is positively correlated with sperm length among, but not within, species. These different responses to sperm competition at intra- and interspecific levels provide a simple, powerful explanation for equivocal results from previous studies. Using phylogenetic analyses, we also reconstructed the probable evolutionary route of trait evolution in this taxon, and show that, in response to increases in the magnitude of sperm competition, the evolution of sperm traits in this clade began with the evolution of faster (thus, more competitive) sperm.

Ejaculate Allocation and Sperm Characteristics Differ among Alternative Male Types in a Species of Fish with Cooperation and Competition among Unrelated Males.

Sexual selection arising from sperm competition has driven the evolution of immense variation in ejaculate allocation and sperm characteristics not only among species, but also among males within a species. One question that has received little attention is how cooperation among males affects these patterns. Here we ask how male alternative reproductive types differ in testes size, ejaculate production, and sperm morphology in the ocellated wrasse, a marine fish in which unrelated males cooperate and compete during reproduction. Nesting males build nests, court females and provide care. Sneaker males only "sneak" spawn, while satellite males sneak, but also help by chasing away sneakers. We found that satellite males have larger absolute testes than either sneakers or nesting males, despite their cooperative role. Nesting males invested relatively less in testes than either sneakers or satellites. Though sneakers produced smaller ejaculates than either satellite or nesting males, we found no difference among male types in either sperm cell concentration or sperm number, implying sneakers may produce less seminal fluid. Sperm tail length did not differ significantly among male types, but sneaker sperm cells had significantly larger heads than either satellite or nesting male sperm, consistent with past research showing sneakers produce slower sperm. Our results highlight that social interactions among males can influence sperm and ejaculate production.

Ovarian fluid allows directional cryptic female choice despite external fertilization.

In species with internal fertilization, females can favour certain males over others, not only before mating but also within the female's reproductive tract after mating. Here, we ask whether such directional post-mating (that is, cryptic) female mate choice can also occur in species with external fertilization. Using an in vitro sperm competition experiment, we demonstrate that female ovarian fluid (ovarian fluid) changes the outcome of sperm competition by decreasing the importance of sperm number thereby increasing the relative importance of sperm velocity. We further show that ovarian fluid does not differentially affect sperm from alternative male phenotypes, but generally enhances sperm velocity, motility, straightness and chemoattraction. Under natural conditions, female ovarian fluid likely increases the paternity of the preferred parental male phenotype, as these males release fewer but faster sperm. These results imply females have greater control over fertilization and potential to exert selection on males in species with external fertilization than previously thought possible.

Relatedness and helping in fish: examining the theoretical predictions.

Many studies have attempted to explain the evolution of cooperation, yet little attention has been paid to what factors control the amount or kind of cooperation performed. Kin selection theory suggests that more cooperation, or help, should be given by relatives. However, recent theory suggests that under specific ecological and demographic conditions, unrelated individuals must 'pay to stay' in the group and therefore may help more. We tested these contrasting predictions using the cooperatively breeding fish, Neolamprologus pulcher, and found that the degree of work effort by helpers depended on which helping behaviours were considered and on their level of relatedness to the breeding male or female. In the field, helpers unrelated to the breeding male performed more territory defence, while helpers unrelated to the breeding female contributed less to territory defence. In the laboratory, unrelated group members helped more. Our work demonstrates that a number of factors in addition to kinship shape cooperative investment patterns.

Sharing of potential nest sites by Etheostoma olmstedi males suggests mutual tolerance in an alloparental species.

When reproductive competitors tolerate or cooperate with one another, they may gain particular benefits, such as collectively guarding resources or attracting mates. Shared resources may be those essential to reproduction, such as a breeding site or nest. Using the tessellated darter, a species where males but not females compete over potential nest sites, we examined site use and sharing under controlled conditions of differing competitor density. Sharing was observed even when competitor density was low and individuals could have each occupied a potential nest site without same-sex sharing. Males were more likely to share a nest site with one other when the difference in size between them was larger rather than smaller. There was no evidence that female sharing was dependent on their relative size. Fish were generally more likely to use and share larger sites, in accordance with the greater relative surface area they offered. We discuss how one or both sharing males may potentially benefit, and how male sharing of potential nest sites could relate to female mating preferences. Tessellated darter males are known to provide alloparental care for eggs but this occurs without any social contact between the alloparent and the genetic father of the young. Thus, the suggestion that they may also share sites and maintain social contact with reproductive competitors highlights the importance of increased focus on the potential complexity of reproductive systems.