Paternal inheritance of growth in fish pursuing alternative reproductive tactics

In species with indeterminate growth, age‐related size variation of reproductive competitors within each sex is often high. This selects for divergence in reproductive tactics of same‐sex competitors, particularly in males. Where alternative tactics are fixed for life, the causality of tactic choice is often unclear. In the African cichlid Lamprologus callipterus, large nest males collect and present empty snail shells to females that use these shells for egg deposition and brood care. Small dwarf males attempt to fertilize eggs by entering shells in which females are spawning. The bourgeois nest males exceed parasitic dwarf males in size by nearly two orders of magnitude, which is likely to result from greatly diverging growth patterns. Here, we ask whether growth patterns are heritable in this species, or whether and to which extent they are determined by environmental factors. Standardized breeding experiments using unrelated offspring and maternal half‐sibs revealed highly divergent growth patterns of male young sired by nest or dwarf males, whereas the growth of female offspring of both male types did not differ. As expected, food had a significant modifying effect on growth, but neither the quantity of breeding substrate in the environment nor ambient temperature affected growth. None of the environmental factors tested influenced the choice of male life histories. We conclude that in L. callipterus growth rates of bourgeois and parasitic males are paternally inherited, and that male and female growth is phenotypically plastic to only a small degree.     

Description of alternative male reproductive tactics in a shell-brooding cichlid, Telmatochromis vittatus, in Lake Tanganyika

Telmatochromis vittatus (Cichlidae) is a Tanganyikan substrate brooder which spawns in the gastropod-shell nests of a cichlid, Lamprologus callipterus. We describe male reproductive tactics of T. vittatus in and around the shell nests, where males of various sizes were found. Based on utilization patterns of the shell nests, interactions among males, and spawning behaviors, males could be categorized into four types based on reproductive tactics and in order of body size: sneaker males, satellite males, territorial males and piracy males. Size range of males in tactic groups rarely overlapped. Territorial males defended shell nests harboring multiple females, but during pair-spawning they were occasionally taken over by large piracy males that visited several nests repeatedly. Small sneaker males darted to pair-spawning territorial males and might ejaculate sperm. Satellite males did not perform parasitic spawning but pair-spawned in a single shell outside the nests. Spawning of satellite males was infrequently parasitized. The largest gonado-somatic index (GSI) was found in sneaker males followed by piracy males, territorial males and satellite males, suggesting that gonadal investment of males using the four tactics may be consistent with intensity or risk of sperm competition.     

Alternative reproductive tactics in snail shell‐brooding cichlids diverge in energy reserve allocation

Life history theory predicts that the amount of resources allocated to reproduction should maximize an individual's lifetime reproductive success. So far, resource allocation in reproduction has been studied mainly in females. Intraspecific variation of endogenous energy storage and utilization patterns of males has received little attention, although these patterns may vary greatly between individuals pursuing alternative reproductive tactics (ARTs). ARTs are characterized by systematic variation of behavioral, physiological, and often morphological traits among same‐sex conspecifics. Some individuals may rely on previously accumulated reserves, because of limited foraging opportunities during reproduction. Others may be able to continue foraging during reproduction, thus relying on reserves to a lesser extent. We therefore predicted that, if male tactics involve such divergent limitations and trade‐offs within a species, ARTs should correspondingly differ in energy reserve allocation and utilization. To test this prediction, we studied short‐term and long‐term reserve storage patterns of males in the shell‐brooding cichlid Lamprologus callipterus. In this species, bourgeois males investing in territory defense, courtship, and guarding of broods coexist with two distinct parasitic male tactics: (1) opportunistic sneaker males attempting to fertilize eggs by releasing sperm into the shell opening when a female is spawning; and (2) specialized dwarf males attempting to enter the shell past the spawning female to fertilize eggs from inside the shell. Sneaker males differed from other male types by showing the highest amount of accumulated short‐term and long‐term fat stores, apparently anticipating their upcoming adoption of the nest male status. In contrast, nest males depleted previously accumulated energy reserves with increasing nest holding period, as they invest heavily into costly reproductive behaviors while not taking up any food. This conforms to a capital breeder strategy. Dwarf males did not accumulate long‐term fat stores at all, which they can afford due to their small behavioral effort during reproduction and their continued feeding activity, conforming to an income breeder strategy. Our data confirm that the resource storage patterns of males pursuing ARTs can diverge substantially, which adds to our understanding of the coexistence and maintenance of alternative reproductive patterns within species.     

Alternative mating tactics and acoustic behaviour in the grass goby Zosterisessor ophiocephalus: a behavioural analysis of the interaction between the parasitic and the bourgeois male

In this study the behavioural interaction between the bourgeois and the parasitic male of the grass goby, Zosterissor ophiocephalus , is investigated during spawning in the laboratory. Large grass goby males care for the eggs (bourgeoise males), whereas small males are believed to adopt an alternative mating tactic. The behavioural interaction between one large male spawning inside an artificial nest (a large plastic box buried in the sand provided with two entrance tubes opening on the substrate) and one small male, was investigated in five small male‐large male pairs. The small male performed parasitic activity in four replicates. The main activity of the parasitic male was staying still on the substrate by one nest opening (Waiting), usually followed by one or more attempts to enter the nest. Waiting was performed repeatedly by the parasitic male at both nest openings across the spawning period. The activity of the large male inside the nest consisted mainly of switching between spawning‐related activities ( e.g . Upside‐down) and standing still inside one of the two entrance tubes of the nest (Patrolling). The analysis of temporal relationship among behavioural activities showed a positive relationship between the occurrence of Waiting and Patrolling in 3 out of 4 replicates, with Patrolling occurring more frequently at the nest opening at which the parasitic male was Waiting. Only 20% of all the intrusion attempts observed in the five replicates were successful, i.e . the parasitic male entered the burrow and performed egg‐fertilization movements. A significant emission of sounds by the bourgeois male, mostly associated with Patrolling, was documented. The function of the bourgeois male sound production during spawning is discussed.     

Bourgeois Males of the Peacock Blenny,Salaria pavo,Discriminate Female Mimics from Females?

In a Portuguese population of Salaria pavo, two types of reproductively active males occur: large bourgeois males that defend nests and have fully developed secondary sex characters (SSC) and small sneaker males that mimic the females’ morphology and behaviour to approach nests and parasitize fertilizations. These two alternative reproductive tactics are sequential, as sneakers develop into bourgeois males. We investigated whether bourgeois males were able to discriminate between sneakers and females of different sizes. In a laboratory experiment bourgeois males were sequentially presented with a female and a sneaker matched for size. Complementary field observations were conducted on the interactions between females and sneakers with bourgeois males. If bourgeois males discriminated females from sneakers, we predicted that they should direct more aggressive behaviours towards sneakers and more courtship acts towards females. In general, bourgeois males courted and attacked small females and sneakers equally. However, large sneakers were courted less and attacked more than large females. Larger sneakers, beginning to develop SSC, were attacked more and courted less by the bourgeois male than smaller sneakers, and larger females were attacked less and courted more than smaller females. These results strongly suggest that only small female‐mimicking males were able to deceive bourgeois males. In S. pavo, if the sneakers’ fertilization success correlates with their female‐mimicking ability, a fitness decrease with an increasing body size can be predicted.     

Breeding success of male brook trout (Salvelinus fontinalis) in the wild

Competition for females generally results in some males adopting alternative reproductive tactics to acquire matings. For fish, the ecological and evolutionary consequences of these tactics are not well understood because of an inability to link directly the interactions of individuals on the breeding grounds with genetic data. This study combines behavioural observations with genetic estimates of male reproductive success within an intensively studied wild population of lacustrine brook trout (Salvelinus fontinalis). Male brook trout exhibit a conditional reproductive strategy with small males adopting a peripheral position to that of larger dominant males in their proximity to spawning females. Parentage analysis of eggs collected from wild redds confirmed the reproductive success of individual males. Males relegated to peripheral positions during spawning participated frequently in spawning events, but in most cases the first male to spawn was the sole contributor, and no more than two males contributed successfully to a single brood. While behavioural observations of salmonines suggests that reproduction is partitioned among males in a manner dependent upon body size and proximity to spawning females, the genetic evidence from this study suggests a more limited distribution of reproductive success in the field. The genetic contributions of male brook trout are highly skewed towards larger males for this population. A review of the salmonine literature suggests little difference in individual reproductive success for males exhibiting size-related tactics within a conditional mating strategy vs. precocial maturation. Collectively, these genetic studies provide new insights on the evolution of alternative life histories among salmonines.     

Reproductive parasitism: male and female responses to conspecific and heterospecific intrusions at spawning in a mouth‐brooding cichlid Ophthalmotilapia ventralis

A rare form of alternative reproductive behaviour without simultaneous parasitic spawning was observed in Ophthalmotilapia ventralis, a lekking mouth‐brooding cichlid from Lake Tanganyika. Floater males attempted to sneak opportunistically into the territory to actively court the female, while the owner (bourgeois male) defended the territory against other potential intruders. Floater males had more body fat than territory owners and generally higher condition factors. In field experiments, the response of bourgeois males and courted females was tested towards floaters and egg predators (a catfish Synodontis multipunctatus) present in the territories. Territory owners responded aggressively particularly to floaters, and female responsiveness to bourgeois male courtship tended to decline when floaters were present. The potential influence of reproductive parasitism on sexual selection in mouth‐brooding cichlids is discussed.     

The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes

Among vertebrate classes, fishes exhibit by far the greatest variability in competitive and cooperative behaviors in male reproduction. Scramble competition between reproductive males is one possibility. Another possibility occurs when resources, mates, or locations can be monopolized, in which case males may invest in primary access to fertilizations by adopting a "bourgeois" strategy, or they may employ alternative mating tactics to evade the reproductive monopoly of other males. Adaptations in morphology, physiology, and behavior to bourgeois and alternative phenotypes are highly divergent. Here I review the functional characteristics that differ between bourgeois and parasitic phenotypes, and discuss the variability of alternative reproductive tactics at the levels of plasticity, determination, and selection. Examples will illustrate the importance of ecology, and will suggest that variation in reproductive tactics is largely adaptive. Behavioral solutions to competition for mates and fertilizations often involve agonistic behavior and conflict, but also cooperation among competitors (e.g., when subordinate males pay a price to bourgeois males for gaining access to fertilizable eggs). Application of molecular genetic tools has helped to uncover intricate sexual and social relationships in various fish species, including species that display some of the most complex reproductive and social patterns known among the vertebrates.     

Body size evolution of a shell‐brooding cichlid fish from Lake Tanganyika

The substrate‐brooding cichlid fish Telmatochromis temporalis in Lake Tanganyika demonstrates a simple example of ecological speciation between normal and dwarf morphs through divergent natural selection on body size. The dwarf morph most likely evolved from the ancestral normal morph; therefore, elucidating the evolution of its small body size is a key to understanding this ecological speciation event. Previous studies suggest that the small body size of the dwarf morph is an adaptation to the use of empty snail shells as shelters (males) and spawning sites (females), but this idea has not been fully evaluated. Combining original and previously published information, this study compared likelihood values to determine the primary factor that would be responsible for regulating the body size of the dwarf morph. Male body size is most likely regulated by the ability to turn within shells, which may influence the predation avoidance of adult fish. Females are smaller than males, and their body size is most likely regulated by the ability to lay eggs in the small spaces within shells close to the shell apices where predation risk on eggs is lower. This study provides new evidence supporting the hypothesis that different natural selection factors affected body size of the different sexes of the dwarf morph, which has not been reported in other animal species.     

Social network predicts loss of fertilizations in nesting males of a fish with alternative reproductive tactics

Alternative reproductive tactics (ARTs) evolve when there is strong intra-sexual competition between conspecifics for access to mates. Typically, larger “bourgeois” males reproduce by securing the access to reproductive resources while smaller “parasitic” males reproduce by stealing fertilizations from larger males. A number of factors can influence the reproductive success of each tactic, including intrinsic (e.g. size) and extrinsic (e.g. tactic relative frequency) variables. An example where plastic ARTs occur is the peacock blenny Salaria pavo, with large males reproducing by defending nests and attracting females (bourgeois tactic) and small males reproducing by achieving sneaked fertilizations (parasitic tactic). In this study, we conducted field observations on individually tagged animals to determine their social network and collected eggs from 11 nests to determine the fertilization success of each male tactic. Paternity estimates for 550 offspring indicated an average fertilization success for nest-holder males of 95%. Nest-holder male morphological traits and social network parameters were tested as predictors of fertilization success, but only the number of sneakers present in the nest-holder’s social networks was found to be a predictor of paternity loss. Although male morphological traits had been previously found to be strongly correlated with reproductive success of nest-holder males, as measured by the number of eggs collected in the male’s nest, no correlation was found between any of the measured morphological traits and fertilization success for these males. The results suggest a stronger influence of the social environment than of morphological variables in the proportion of lost fertilizations by nest-holder males of this species.     

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.     

Behavioral Tactics of Male Sockeye Salmon (Oncorhynchus nerka) under Varying Operational Sex Ratios

Previous studies have demonstrated several reproductive-behavior patterns in male salmon, including competitive and sneaking tactics, the formation of hierarchies, and non-hierarchical aggregations around ripe females. Through behavioral observations at varying spatial and temporal scales, we examined the hypothesis that operational sex ratio (OSR) determines male sockeye salmon (Oncorhynchus nerka) distribution and breeding tactics. Patterns of male distribution and behavior varied over both coarse and fine scales, associated with apparent shifts in reproductive opportunities, the physical characteristics of the breeding sites, and the deterioration of the fish as they approached death. Females spawned completely within a few days of arriving on the spawning grounds, whereas males courted the available ripe females from the date of their arrival on the spawning ground until their death. This difference in reproductive lifespans tended to elevate late-season OSRs but was partially counterbalanced by male departures and the arrival of other ripe females. The proportion of males able to dominate access to ripe females decreased and the number of large courting groups increased over the course of the season, apparently related to both increasing OSR and the deteriorating physical condition of males. However, great variation in OSR was observed within the spawning sites on a given day. OSRs were generally higher in shallow than in deep water, perhaps because larger females or more desirable breeding sites were concentrated in shallow water. The aggregations of males courting females were not stable (i.e. many arrivals and departures took place) and male aggression varied with group size. Aggression was most frequent at low OSRs and in groups of intermediate size (2–4 males per female), and much less frequent in larger groups, consistent with the needs of maximizing reproductive opportunities while minimizing unproductive energy expenditure. These results indicate that, while OSR strongly influences male distribution and behavior, other factors such as physical condition, limited movement and habitat choice may also affect male reproductive opportunities.     

Sneak male mating tactics between lampreys (Petromyzontiformes) exhibiting alternative life‐history strategies

Interspecific sneak male mating tactics between paired lamprey species are described for the first time. Although alternative mating tactics among petromyzontids have been described previously, including intraspecific sneak males, the presence of sneak male tactics between parasitic and non‐parasitic forms suggests that high levels of gene flow between putative lamprey species could remain high, despite large body size discrepancies.     

Scallop Size does not Predict Amount or Rate of Induced Sperm Release

Within populations of broadcast spawning marine invertebrates such as scallops, larger animals typically have larger gonads. Presumably, this means those larger males have more sperm to release than small males. However, there has never been a direct test of whether larger males actually release more sperm, at a higher rate, during spawning. To address this, we compared the allometry of induced sperm release with that of reproductive investment (gonad weight) in ripe males of 2 species of scallops, Chlamys bifrons and Chlamys asperrima. We did not find that larger scallops released more sperm or released it faster than small scallops, and were able to reject the hypothesis that instantaneous sperm release was related to body size in the same way as gonad weight. Consequently, we speculate that if larger broadcast spawning males do release more sperm, they may do so by spawning on more occasions within a reproductive season.     

Scallop Size does not Predict Amount or Rate of Induced Sperm Release

Within populations of broadcast spawning marine invertebrates such as scallops, larger animals typically have larger gonads. Presumably, this means those larger males have more sperm to release than small males. However, there has never been a direct test of whether larger males actually release more sperm, at a higher rate, during spawning. To address this, we compared the allometry of induced sperm release with that of reproductive investment (gonad weight) in ripe males of 2 species of scallops, Chlamys bifrons and Chlamys asperrima. We did not find that larger scallops released more sperm or released it faster than small scallops, and were able to reject the hypothesis that instantaneous sperm release was related to body size in the same way as gonad weight. Consequently, we speculate that if larger broadcast spawning males do release more sperm, they may do so by spawning on more occasions within a reproductive season.     

Observations on interbreeding between dwarf and normal arctic charr,Salvelinus alpinus,from Stora Rösjön,central Sweden

Synopsis The spawning behaviour of dwarf and normal arctic charr, Salvelinus alpinus, was studied through trough observations in October 1988. The experimental fish consisted of reared, three-summer old progeny of artificially bred dwarf and normal charr from an isolated body of water in central Sweden. The spawning behaviour of three normal female charrs was studied and video-recorded. The study showed that the arctic charr is potentially polyandric both within and between forms. The normal female was courted and mated both by normal and dwarf males. It was also noted that antagonistic behaviour on behalf of the female was much more common towards dwarf males than normal males. Guarding tactics were only observed in normal males, whereas sneaking tactics were employed both by dwarf and normal males. The dwarf as well as normal males mated the female charr either by courting the female or by joining the spawning fish at oviposition. Only dwarf males were observed resting silently on the bottom close to the redd.     

Male Parasitic Spawning in Two Species of Triplefin Blenny (Tripterigiidae): Contrasts in Demography, Behaviour and Gonadal Characteristics

Axoclinus nigricaudus and A. carminalis are blennioid fishes from the Gulf of California, Mexico. Males show alternative mating tactics; territorial individuals attract females while non-territorial individuals parasitically spawn with territorial males' females. Demography and gonadal characteristics were related to the degree of parasitic spawning (sperm competition) within and between species. Males of both species showed bimodal size distributions that largely reflected the two tactics. Territorial males spawned much more frequently than non-territorial males, but parasitic spawning was significant. Non-territorial males were more common and rates of parasitic spawning were much higher in A. nigricaudus indicating that it experienced higher sperm competition. In agreement with sperm competition theory, relative testis weight was greater in A. nigricaudus. In A. nigricaudus, the majority of parasitic matings were by non-territorial males, whereas in A. carminalis, both male-types parasitised frequently. Accordingly, only in A. nigricaudus did non-territorial males have relatively heavier testis than territorial males. In both species the testicular gland, that produces accessory products for sperm transfer, was large in territorial males, but small or undeveloped in non-territorial males suggesting male-types differ in fertilisation mode.     

Male reproductive competition in spawning aggregations of cod (Gadus morhua, L.)

Reproductive competition may lead to a large skew in reproductive success among individuals. Very few studies have analysed the paternity contribution of individual males in spawning aggregations of fish species with huge census population sizes. We quantified the variance in male reproductive success in spawning aggregations of cod under experimental conditions over an entire spawning season. Male reproductive success was estimated by microsatellite-based parentage analysis of offspring produced in six separate groups of spawning cod. In total, 1340 offspring and 102 spawnings distributed across a spawning season were analysed. Our results show that multiple males contributed sperm to most spawnings but that paternity frequencies were highly skewed among males, with larger males on average siring higher proportions of offspring. It was further indicated that male reproductive success was dependent on the magnitude of the size difference between a female and a male. We discuss our results in relation to the cod mating system. Finally, we suggest that the highly skewed distribution of paternity success observed in cod may be a factor contributing to the low effective population size/census population size ratios observed in many marine organisms.     

Group spawning results from the streaking of small males into a sneaking pair: male alternative reproductive tactics in the threespot wrasse Halichoeres trimaculatus

In many protogynous wrasses, large males with bright coloration (terminal phase males, TP males) establish mating territories and pair-spawn with females. In contrast, small primary males with drab coloration (initial phase males, IP males) are non-territorial and adopt three alternative reproductive tactics—group spawning, streaking, and sneaking. We investigated how IP males of the threespot wrasse Halichoeres trimaculatus use these tactics in different situations. The mating frequency of the IP males was positively correlated with their courtship frequency, but not with their body size. Larger IP males tended to attack the smaller ones at the mating sites. This indicates that the larger IP males attempted to exclude the smaller ones from mating with the intention of minimizing the number of IP males involved in group spawning and ultimately leading to pair spawning (sneaking). However, the larger IP males were unable to completely exclude the smaller males because the intensity of the attack by the larger IP males was weak. Consequently, the smaller IP males could easily streak into the sneaking of larger IP males, thereby resulting in group spawning.     

Repeated matings and sperm depletion in the freshwater crayfish Austropotamobius italicus

1. In sexually reproducing organisms, the energetic costs of spermatogenesis can be considerable, and can limit the reproductive potential of the males. In species where males mate more than once during the reproductive season, the costs of sperm production are generally predicted to result in a decrease of ejaculate size and quality with successive fertilizations. 2. In this study we examined the variation in ejaculate size among successive fertilizations in a long‐lived freshwater crayfish species, Austropotamobius italicus. 3. Sexually active adult males of various sizes were allowed to mate repeatedly with different females on consecutive days. Trials for a given male ended when he copulated but did not release any sperm or refused to mate. 4. Males fertilized between 0 and 4 females, and most (42.5%) fertilized a single female. The overall number of females fertilized by a given male decreased with increasing male body size. Ejaculate size decreased markedly with consecutive fertilizations in a similar fashion among both large and small males, while simultaneously increasing with female body size. The total ejaculate size over successive fertilizations decreased with increasing male size. 5. Our study indicates that either sperm production or release involves non‐trivial costs in freshwater crayfish, and suggests that large/old males may face greater difficulties in gamete release than small/young ones, as shown by the lower number of females fertilized by large compared with small males, which may reflect the ongoing senescence of their reproductive performance.