Parasitic spawning in sand gobies: an experimental assessment of nest-opening size, sneaker male cues, paternity, and filial cannibalism

Sneaking is common in nest-building fish with paternal care,but the role of nest-opening size in protecting against entryby sneaker males has never been tested before. Using the sandgoby (Pomatoschistus minutus), a fish with exclusive paternalcare, experimental manipulations of nest openings provided nosupport for the hypothesis that nest openings serve as physicalor visual defense or that sneaker males prefer to parasitizenests with wide openings. Female mating preference was alsonot influenced by nest-opening size. However, female courtshipbehavior and visibility were important cues for sneaker males.Most sneak entries occurred when the nest holder was occupiedwith courtship, chasing another sneaker male or nest building.In half the cases of observed sneak entry, the sneaker malefertilized eggs, also when sneaking only occurred before spawning.Sneak entry and its duration were good estimates of stolen paternity,but neither sneak entries nor degree of fertilizations werecorrelated with filial cannibalistic behavior. Testes size didnot explain parasitic spawning success in replicates with geneticallydetermined sneaking. However, all sneaker males without breedingcoloration had huge testes and small sperm duct glands, whereasnest-holding males had small testes and large sperm duct glands,and sneaker males with breeding coloration were intermediate.     

Costs of egg ventilation for male common gobies breeding in conditions of low dissolved oxygen

This study examines the effects of harsh environmental conditions on life history trade-offs in parental care in a marine fish, the common goby, Pomatoschistus microps. We compared male parental care and hatching success over two sequential brood cycles in fish breeding in conditions of either low dissolved oxygen or normal levels of oxygen. Males compensated for a low oxygen environment by increasing the time they spent fanning water over their eggs, as well as their fanning tempo. They also increased the frequency of egg-directed activities and decreased nest-building activities. Males in the low oxygen treatment lost more weight than control fish during the first spawning, and were more likely to abandon care during the second spawning. Males that completed care under low oxygen conditions did not differ from control males in the hatching success of their offspring or the size of young at hatching, but hatching started on average 1 day later. Thus, greater parental allocations to offspring while breeding in a harsh environment led to reduced future allocations. Copyright 1999 The Association for the Study of Animal Behaviour.     

Alternative reproductive tactics and courtship in the common goby

In the marine common goby Pomatoschistus microps , males either build nests and attract females to spawn or act as sneakers, forcing themselves into other males' nests during mating, to fertilize some of the eggs in the clutch. The reproductive tactics of small males were studied in the presence of surplus nest material and an excess of gravid females, while a larger, nestholding male spawned with a female. Of 24 small males, 13 only attempted to sneak, seven only courted females and/or spawned in their own nest, and four performed both behaviours. The small males who attracted females successfully were significantly larger than the ones who failed to do so. Females had been courting the small male more often when he subsequently spawned in his own nest, than when he did not get a female. The small males did not court the females very frequently, and their courtship rate did not depend on whether or not they attracted females. Instead, female courtship behaviour may be a cue for a male either to spawn as a nest holder or become a sneaker. The study pointed out the importance of female behaviour for male reproductive tactics, which could be more important in fish than is known currently.     

Big is better: the importance of size for reproductive success in male Pomatoschistus minutus (Pallas) (Pisces, Gobiidae)

The sand goby, Pomatoschistus minutus , was used in aquarium experiments to study the importance of body size for the ability of males to gain access to nest sites and mates. When several male and female P. minutus were allowed to reproduce together, on average, half of the males built nests, and half of those males obtained eggs in their nests. Males with nests were significantly larger than males without nests, and nests with eggs belonged to males larger than the males with empty nests. In another experiment, when two males were competing for one nest, the largest male occupied the nest when both fish were put into the aquarium simultaneously. However, when the smaller male had been allowed to establish a nest before the larger male was introduced, the small male could usually retain the nest. Males with a body length < 50 mm did not build nests at all in the early part of the breeding season. In female choice experiments, no preference for larger males was found. Thus, male-male competition for nest sites and behavioural differences between different sized males seem to be the main factors influencing the non-random mating success in male P. minutus.     

Phenotypic variation between dimorphic males in corkwing wrasse

The age-frequency distributions for sneaker males (individuals with female secondary sexual characters) and territorial males (individuals with typical male sexual characters) of corkwing wrasse Symphodus melops in a Swedish population did not differ. Otolith analysis revealed that sneaker males were smaller than their territorial male counterparts as juveniles, but there was no evidence of a clear-cut threshold to determine the subsequent reproductive patterns. Thus, the expression of male morph in corkwing wrasse most likely is related to early growth pattern and the different morphs could be fixed for life. Adult sneaker males in general were smaller than territorial males of the same age. The relative gonad size and the abdomen in sneaker males were substantially enlarged compared with territorial males, but there was no difference in gonad water content between the two types of males. Sneaker males weighed less in relation to their length than territorial males. These results support theoretical sperm competition models which predict that the male morph with reduced attractiveness to females (i.e. sneakers) should invest more into spermatogenesis in order to achieve fertilization than the attractive male morph (i.e. territorial males).     

Tactic changes in dusky frillgoby Bathygobius fuscus sneaker males: effects of body size and nest availability

Field and laboratory studies were conducted to examine the effects of nest availability and body size on changes in male mating tactics from sneaking to nest‐holding in the dusky frillgoby Bathygobius fuscus. In the field, the body size of nest‐holding males decreased from early to mid‐breeding season, suggesting the possibility of a change in the tactics of sneaker males to nest‐holding. Many sneaker males did not use vacant spawning nests even when size‐matched nests were available, but they continued to reproduce as sneakers. Similarly, in aquarium experiments with available vacant nests, some sneaker males became nest‐holders irrespective of their body size, but some did not. These results showed that nest availability is not a limiting factor for changes in tactics by sneaker males in this species. Because tactic‐unchanged sneaker males were co‐housed with larger nest‐holding males in the tanks, the body size of nearby nest‐holding males may have affected the decision to change tactics for sneaker males. Moreover, smaller individuals among tactic‐changed males tended to spend more time until spawning, probably because they had relatively larger costs and smaller benefits of reproduction as nest‐holding males compared to larger males.     

A trade-off generated by sexual conflict: Mediterranean wrasse males refuse present mates to increase future success

A variety of mechanisms, including intrasexual competition,intersexual conflict, and physiological constraints, can explainpatterns of reproduction and the adaptive value of specificbehaviors. In a Mediterranean wrasse, Symphodus ocellatus (Labridae),large, nesting males occasionally refuse to spawn with willingfemales in the presence of small, sneaker males. We exploredthe possible adaptive significance of this behavior. Nestingmales refuse females despite the fact that it reduces theirimmediate mating success. This nesting-male behavior also decreasesfemale and sneaker mating success and occurs when sneaker malessurround the nest. Experiments that decreased the number ofsneakers around nests showed that nesting males respond immediatelyto mating opportunities when fewer sneakers are present, andthus they are not simply constrained by a lack of energy orlack of sperm. Experiments that increased the number of sneakersat the nest caused nesting males initially to refuse spawningopportunities, followed by a subsequent decrease in sneakerpresence and an increase in mating rate. We propose that thisbehavior is the result of a trade-off between immediate matingsuccess and future reproduction created by competition betweenmales and conflict between the sexes. Males reduce their immediatemating success by reducing spawning at the nest; sneaker malessubsequently leave, and this decreases mate competition forthe nesting male. Unresponsiveness of nesting males also causessexual conflict between females and nesting males over mating.We argue that this behavior and the existence of a trade-offcan only be understood by examining intersexual conflict andintrasexual competition simultaneously.     

Ejaculate of sneaker males is pheromonally inconspicuous in the black goby,Gobius niger (Teleostei,Gobiidae)

The black goby, Gobius niger, shows alternative male mating tactics, i.e., parental and sneaker males. Males release a sexual pheromone that attracts females and stimulates aggressive displays in males. This pheromone is produced by the mesorchial gland, a structure well developed in parental males but markedly undeveloped in sneakers. We measured the behavioral response of parental males to the ejaculates of males performing different reproductive tactics. Parental males reacted to the ejaculate of other parental males, with stereotypic aggressive behaviors, but not to the ejaculate of sneakers; consequently sneaker male ejaculate appears to be pheromonally inconspicuous.     

Complex adaptive traits between mating behaviour and post-copulatory sperm behaviour in squids

Emergence of male dimorphism within a species is the evolutionary process of disruptive selection. In squids, two types of male mating behaviour, known as alternative reproductive tactics (ARTs), are causally associated with adult body size. Males inseminate promiscuously with the same females; large “consort” males internally, and small “sneaker” males externally. Previously we found that in Heterololigo bleekeri, sneaker (but not consort) spermatozoa are able to swarm by sensing self-emitted CO₂. This suggests that a swarming trait might have arisen in sneakers as a “sperm cooperation” strategy among sibling sperm in order to compete with consort males, or as a consequence of adaptation to external fertilization. To address these possibilities, we examined six species where three patterns of insemination are present, namely, only internal, only external, or both ARTs. In three species that employ both ARTs (H. bleekeri, Loligo reynaudii and Uroteuthis edulis), sneaker spermatozoa always exhibited self-swarming capacity. In Idiosepius paradoxus and Todarodes pacificus, which use only external insemination, spermatozoa formed a swarm. However, in Euprymna morsei, which use only internal insemination, sperm were unable to swarm. These results suggest that the self-swarming trait is likely to be linked to the mode of insemination rather than the alternative strategy used by sneaker males. Thus we propose a new hypothesis in which cooperative sperm behaviour has evolved not only through kin selection against sperm competition risks, but also through adaptation to the insemination/fertilization environment.     

The importance of sperm competition risk and nest appearance for male behavior and female choice in the sand goby, Pomatoschistus minutus

To test if an increased sperm competition risk affects malebehavior and mating decisions of both sexes, we performed twoexperiments using the sand goby, Pomatoschistus minutus, a nest-buildingfish with exclusive paternal care. In our first experiment,a nest-holding male, with a confined female, was sequentiallyexposed to a vial with a sneaker male or an empty vial. Whilemale courtship, nest building, displacement fanning, and timeoutside the nest were unaffected, individual males showed ahigher mucus preparation effort inside the nest in the presenceof a sneaker male than when alone. We found such mucus to containsperm, thus clearly suggesting an importance in sperm competition.In our second experiment, a female was free to spawn with twodifferent males, one of which was exposed to a confined sneakermale. Male mating success was not affected by the presence ofa sneaker male. However, the volume of sand the male had puton his nest was positively associated with female spawning decision,while nest-opening width was not. In a partial correlation offive traits thought to attract females (nest-opening width,sand volume, male courtship display, displacement fanning, andmale size), males that fanned well were found to also buildlarge nests or display intensely, but not both. This indicatesthat rather than being jacks-of-all-trades, individual malesfocus on a subset of traits for attracting females.     

Male mating success in relation to food availability in the common goby

In a feeding experiment with the common goby Pomatoschistus microps , there was no female preference for well-fed males, although these males had a higher mating success. This suggests that care should be taken about drawing conclusions regarding mate choice and mating success based on mate preference tests alone.     

Intersexual copying by sneaker males of the peacock blenny

In general, animals prefer to mate with individuals they have observed being courted or in close association with sexual partners. This phenomenon of mate copying has been demonstrated in several species, but so far no study has provided substantial evidence that it is adaptive. Furthermore, mate copying has been viewed only in the context of females copying other females or males copying other males. In the peacock blenny, Salaria pavo, parasitic males (sneakers) may gain an advantage by copying the association patterns of females with bourgeois males (large males that defend nests). We tested the sneaker's preference for one of two males and subsequently presented the nonpreferred male to the sneaker in the company of females, while the preferred male was presented alone. If the association of females with bourgeois males influences the sneaker's preference, we predicted the sneaker would spend more time close to the nonpreferred male, when females were no longer present. We found that (1) sneakers preferred to associate with the larger of the two males and (2) when the previously nonpreferred male was presented in the company of females the sneakers tended to approach that male sooner, although not significantly so, and to spend more time close to it. Thus, parasitic males seem to choose host males both by independent mechanisms (larger males were preferred) and by nonindependent mechanisms (males observed with females were preferred). We discuss the adaptive value of sneakers choosing males by each of these mechanisms. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Sex-role reversal revisited: choosy females and ornamented, competitive males in a pipefish

In the pipefish Syngnathus typhle sex roles are reversed, thatis, females compete more intensely than males over mates. However,competition over mates among individuals of one sex does notnecessarily prevent members of that same sex from being choosy,and choosiness in the other sex does not prevent competitionwithin it. In an experiment we allowed a female pipefish tochoose freely between two males, after which we released themales and let the three interact. Comparisons with earlier resultsshow that both sexes courted partners and competed with consexuals.However, females courted more often than did males, and courtshipwas more frequent in treatments involving large individualsthan in treatments with small individuals. Males competed amongthemselves for access to mates but for a shorter duration thanfemales in the same situation. Males displayed an ornament towardsfemales but not to males during mating competition. Females,however, used their ornament in both contexts. Females did notalways mate with the male of their previously made choice, whichwe interpret as females being constrained by male-male competition,male motivation to mate, or both. Thus, in this sex-role reversedspecies, mate choice in the more competitive sex may be circumventedand even overruled by mate competition and mating willingnessin the least competitive sex. Hence, sex roles should not beconsidered as sexes being either choosy or competitive but ratherthat males and females may exhibit different combinations ofchoice and competition.     

Unexpected female preference for smaller males in the marbled goby Pomatoschistus marmoratus

The study tested the role of body size and of nest size in female mate choice in the marbled goby, Pomatoschistus marmoratus. The results show a female preference for smaller males, supporting the idea that smaller males may be preferred to larger ones in the absence of male–male competition. No effect of nest size was detected, suggesting that other nest characteristics, beyond nest size, may be implicated.     

Social learning in nest-building birds: a role for familiarity

It is becoming apparent that birds learn from their own experiences of nest building. What is not clear is whether birds can learn from watching conspecifics build. As social learning allows an animal to gain information without engaging in costly trial-and-error learning, first-time builders should exploit the successful habits of experienced builders. We presented first-time nest-building male zebra finches with either a familiar or an unfamiliar conspecific male building with material of a colour the observer did not like. When given the opportunity to build, males that had watched a familiar male build switched their material preference to that used by the familiar male. Males that observed unfamiliar birds did not. Thus, first-time nest builders use social information and copy the nest material choices when demonstrators are familiar but not when they are strangers. The relationships between individuals therefore influence how nest-building expertise is socially transmitted in zebra finches.     

Disruption of sexual selection in sand gobies (Pomatoschistus minutus) by 17α-ethinyl estradiol, an endocrine disruptor

In aquatic environments, endocrine disrupting chemicals (EDCs) that interfere with the reproductive physiology of males form a threat to the reproduction of populations. This is often manifested as decreased sexual performance or sterility among males. We show that exposure to EDCs can directly affect the mating system of a marine fish, the sand goby (Pomatoschistus minutus). We exposed males for 1 to 4 weeks to two different concentrations (5 ng L^− 1 and 24 ng L^− 1) of 17α-ethinyl estradiol (EE2); a synthetic compound mimicking estrogen and a water control. The sand goby exhibits a polygynous mating system, in which male mating success is typically skewed towards the largest males, resulting in strong sexual selection for increased male size. Our experiment shows that when males have been exposed to EE2, male size has a smaller effect on mating success, resulting in weaker sexual selection on male size as compared to the control. There was an interaction between treatment and exposure time on the expression of vitellogenin and zona radiata protein mRNAs. Males exposed to high EE2 reached much higher expression levels than males exposed to low EE2. Of the somatic markers, the hepatosomatic index was lower in males exposed to high EE2 than in the low EE2 and control males. Our results suggest that exposure to EDCs can have effects on the mating system before physiological changes are observable. These effects can be of profound nature as they interfere with sexual selection, and may in the long run lead to the loss of traits maintained through sexual selection.     

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.     

Yelling for sex: harem males compete for female access in bronze-winged jacanas

Sperm competition in sex-role reversed, polyandrous jacanas is intense because females copulate with multiple male mates before laying each clutch. These males may be unable to attempt to maximize their share of copulations by mate guarding or forcing copulations. Instead, males in polyandrous harems may compete for sexual access to the female by giving a call, termed the 'yell', to attract her. Male bronze-winged jacanas, Metopidius indicus, yelled at higher rates in larger harems, and when the female was further from the yeller or on a comate's territory. Half of all yells were given at mating platforms where all copulations occurred. Males that received the clutch yelled at lower rates during the incubation and chick care periods. Yells attracted the female when she was far from the yeller or with a comate. When the yell of a polyandrous male was broadcast from his territory, the female was more likely to fly to his territory during playback than during control periods. Within polyandrous harems the males that yelled at the highest rates received the most copulations, and three out of four females gave clutches to the male that gave the longest and most frequent yells, so females may have used yells to assess male quality. Intrusions by females, but not males, increased during yell playbacks, and tended to be more frequent on the territories of males with high yell rates. Females may therefore respond to their mates' yells because yells may attract female intruders which may attempt to take over the territory. Copyright 1999 The Association for the Study of Animal Behaviour.     

The influence of oxygen stress on female choice for male nest structure in the common goby

This study examines the role of dissolved oxygen in modifying female mate choice in the common goby, Pomatoschistus microps. Experimental manipulations of nests showed that under normal (saturated) oxygen conditions, females preferred to spawn in nests with the most elaborate construction, that is, those with the most sand on top and the smallest entrance. Such manipulated nests proved less vulnerable to detection by an egg predator, the shore crab, Carcinus maenas, but these small entrances may reduce oxygenation of eggs. Indeed, in a low oxygen environment females with a choice between nests of high build and nests of low build did not significantly prefer either. This may have been due to weakened preference or perhaps detection of a mismatch between the male's parental quality and the increased ventilation needs of eggs when nest entrance sizes are small and ambient oxygen levels are low. When nests were not manipulated, those males that built small entrances fanned their eggs more often, such that hatching success in the absence of a predator was not related to the initial size of the nest entrance area. Thus, under normal oxygen conditions males may initially build nests with the smallest entrance they are capable of ventilating successfully, and females choosing such males gain from nest camouflage. Under low oxygen, the risk that manipulated males may be unable to compensate fully may outweigh such benefits, and females may use other criteria that signal willingness to provide parental care. Copyright 1999 The Association for the Study of Animal Behaviour.     

Genetic mating patterns studied in pools with manipulated nest site availability in two populations of Pomatoschistus minutus

Pomatoschistus minutus show paternal care in a resource defence mating system. We investigated the effect of nest-site availability on parasitic spawning. Each experimental pool contained four potentially nest-building males, four females and nests-sites in shortage (2) or excess (6). Both treatments were conducted in two populations; one with natural nest-sites in excess, one with a nest-site shortage. Microsatellite-DNA revealed that all nest-holders had fertilized most of the eggs they tended. Yet, 35% of the nests contained eggs fertilized by another male and 14.4% of the males had performed parasitic spawning. There was no site or treatment effect. Several females spawned in two nests, which coincided with parasitic spawnings, suggesting a cost to the nest-holder in terms of lost mating success. Nest-holders with and without eggs and non-nesting males all spawned parasitically, generating a significantly lower opportunity for sexual selection compared to if there had been no parasitic spawning.