Alternative Male Mating Tactics Research Articles

Mating system in a small pelagic spawner: field case study of the mandarinfish, Synchiropus splendidus

Mating systems in fishes are extremely diverse, ranging from monogamy to multiple polygamous forms, some of which include alternative male mating tactics within species. The major reproductive mode across approximately 33,000 bony fishes is pelagic-spawning with external fertilization. Despite the dominance of this mode, it is relatively little studied in the field because the greater mobility of larger species typically makes individuals difficult to follow for extensive periods, or to catch and mark. However, smaller, more sedentary pelagic spawners provide excellent opportunities to examine mating system variability in response to environmental conditions. The mandarinfish, Synchiropus splendidus, is a small sedentary pelagic spawner which is accessible to divers. Its complex body markings are distinctive and variable allowing individuals to be identified and followed repeatedly without the need for capturing and marking fish. In over 400 h of underwater surveys, we recorded movements, inter- and intra-sexual behaviors, sex ratios, and the timing and duration of spawning activity of focal fish in predetermined study areas. We concluded that the mandarinfish has a polygamous mating system with pair-spawning. Females are sequentially polyandrous, spawning once nightly or not at all, while males are polygynous, spawning up to 8 times a night. Males and females use loosely defined spawning sites on a daily basis and show flexibility in their tactics through differential movements according to dispersion of individuals, distances between spawning sites and temporally limited daily female receptivity. These results reveal the mandarinfish to be an excellent model species for studying small pelagic spawners in the field.

The Evolution of Social Behaviour

The Evolution of Social Behaviour

Female mating status affects male mating tactic expression in the wolf spider Rabidosa punctulata.

Males and females have conflicting interests on the frequency and outcomes of mating interactions. Males maximize their fitness by mating with as many females as possible, whereas choosy females often reduce receptivity following copulation. Alternative male mating tactics can be adaptive in their expression to a variety of mating contexts, including interactions with a relatively unreceptive mated female. Male Rabidosa punctulata wolf spiders can adopt distinctive mating tactics when interacting with a female, a complex courtship display, and/or a more coercive direct mount tactic that often involves grappling with females for copulation. In this study, we set up female mating treatments with initial trials and then paired mated and unmated females with males to observe both female remating frequencies and the male mating tactics used during the interactions. Males adopted different mating tactics depending on the mating status of the female they were paired with. Males were more likely to adopt a direct mount tactic with already-mated females and courtship with unmated females. Already-mated females were considerably less receptive to males during experimental trials, although they did remate 34% of the time, the majority of which were with males using a direct mount tactic. Whereas males adjusting to these contextual cues were able to gain more copulations, the observation of multiple mating in female R. punctulata introduces the potential for sperm competition. We discuss this sexual conflict in terms of the fitness consequences of these mating outcomes for both males and females.

Octopaminergic system orchestrates combat and mating behaviors: A potential regulator of alternative male mating tactics in an armed beetle

Male-male combats over females and territories are widespread across animal taxa. The winner of a combat gains resources, while the loser suffers significant costs (e.g. time, energy and injury) without gaining resources. Many animals have evolved behavioral flexibility, depending on their nutritional condition and experience, to avoid combat in order to reduce such costs. In these cases, male aggression often correlates with mating behavior changes, that is, the deployment of alternative reproductive tactics. Therefore, uncovering the physiological mechanism that orchestrates combat and mating behaviors is essential to understand the evolution of alternative mating tactics. However, so far, our knowledge is limited to specific behaviors (i.e., fighting or mating) of specific model species. In this study, we used an armed beetle (Gnatocerus cornutus) and hypothesized that one of the key neuromodulators of invertebrate aggression, octopamine (OA), would control male combat and other mating behaviors. Using receptor agonists (chlordimeform and benzimidazole), we showed that the octopaminergic (OAergic) system down-regulated the combat and courtship behaviors, while it up-regulated locomotor activity and sperm size. This suggests that the OAergic system orchestrates a suite of fighting and mating behaviors, thereby implying that correlated behavioral responses to OAergic signaling may have driven the evolution of alternative mating tactics in this beetle.

The overlapping reproductive traits of the two male mating types of the oval squid Sepioteuthis lessoniana

The oval squid Sepioteuthis lessoniana is polyandrous, and a female mates with several males during a spawning season. This has resulted in two alternative male mating tactics in this species. The larger consort males usually use the male-parallel (MP) mating posture to put spermatophores at the opening of the oviduct; the smaller sneaker males predominantly use the male-upturned (MU) mating posture to place spermatophores around the female’s buccal membrane. Since squid eggs are released from the oviduct, MP mating is expected to have a higher fertilization rate than MU mating. Given the fact that these two male mating tactics are largely dependent on the body size of the male relative to the female, it is unclear how the smaller males are able to reproductively compete with the larger males. On analyzing spermatophore and sperm morphology from populations of adult male squids, spermatophore size was found to be positively correlated with mantle length of these squids, but sperm length was negatively correlated with squid mantle length. More importantly, no distinct size dimorphism exists in relation to either spermatophore morphology or sperm morphology. The overlap in size distributions of the spermatophores and sperms of the male squid thus implies that medium-sized males may have flexible reproductive strategies, switching between MP and MU mating tactics depending on the context of the mating event and/or female choice. This presumed behavioral plasticity might increase the reproductive success of these males and maintain the dynamic stability of two alternative mating types in this polyandrous species.

Female Choice Leads to a Switch in Oval Squid Male Mating Tactics.

Oval squids are polyandrous, with one female mating with multiple males during the spawning season. There are two alternative male mating tactics used by Sepioteuthis lessoniana. Larger males place spermatophores at the opening of the oviduct using a male-parallel mating posture, whereas smaller males attach spermatophores around the female buccal membrane using a male-upturned mating posture. If the route of egg transportation is taken into consideration, male-parallel mating would be expected to result in higher fertilization success than male-upturned mating. Although these male mating tactics are largely dependent on the body size of the male relative to that of the female, it is unclear how female choice affects the male's mating tactics and his mating success. Squids are highly visual animals, and they communicate through dynamic body patterning. In the present study, we observed that smaller male squids in captivity would attempt to mate with a larger female using the male-parallel tactic repeatedly, but they failed to be successful most of the time because of a rejection signal by the female. In contrast, when the males switched to the male-upturned tactic, the mating success rate was increased significantly, with much less female rejection signal. This finding suggests that female squids signal their mating receptivity visually and that male squids alter their mating tactics accordingly. This is the evidence to support the hypothesis that the switch in male mating tactics depends on female choice in oval squids and that this is transmitted via visual communication.

Alternative male mating tactics of the endemic Red Sea parrotfish Scarus ferrugineus.

The present study shows that small non-territorial terminal-phase males of the rusty parrotfish Scarus ferrugineus are reproductively active and are comparable with initial-phase males in behaviour, rates of participation during group-spawning and success in streaking into pair spawning. Large territorial terminal-phase males defend contiguous territories for several hours during the morning where they pair spawn with initial-phase females.

Sperm-limited males save ejaculates for future matings when competing with superior rivals

Adjusting ejaculates to sperm competition can lead to sperm limitation. Particularly in polygynous species, males may face a trade-off between investing sperm in current or future mating opportunities. The optimal sperm allocation decision should depend on the relative intensity of sperm competition experienced in a mating sequence. Here we asked how males respond to this trade-off in polygynous fish with alternative male mating tactics, intense sperm competition and sperm limitation. Large bourgeois males of the shell-brooding cichlid Lamprologus callipterus build nests consisting of empty snail shells, in which females spawn and raise offspring. During spawning, nest males release ejaculates into the shell opening. Genetically distinct, parasitic dwarf males enter shells during spawning to fertilize the eggs from inside the shell. These dwarf males were previously shown to be superior sperm competitors to nest males. Here we showed that when spawning with several females simultaneously, nest males reduced the spawning duration for each clutch and the number of ejaculations per female tended to decrease, reflecting sperm limitation. Experimental exposure of nest males to sperm competition with dwarf males reduced the number and duration of ejaculations by roughly half. Hence, when exposed to competition with a superior rival, nest males did not increase their sperm expenditure as predicted by sperm competition risk models, but in fact saved sperm for future mating opportunities as predicted by sperm competition intensity theory. This seems to be adaptive because of the considerable sperm demands in this species, which is partly due to their high degree of polygyny.

Alternative mating tactics and male mating success in two species of fiddler crab

The use of alternative male mating tactics can determine the strength of sexual selection on male traits and have implications for sexual dimorphism. We examined size-based mating success in two species of fiddler crabs where males use each of two alternative tactics to obtain matings. InUca annulipes, larger males were more successful when using the primary mating tactic (burrow mating) but the full size range of males mated when using the secondary tactic (surface mating). InUca urvillei, both burrow and surface mating males were larger than the average sized male in the population. Standardised directional selection gradients indicated that selection on male size was stronger inU. urvilleithanU. annulipes, reflecting the differences between species in male mating success. Our results also showed that sexual size dimorphism was greater in the species with stronger sexual selection on male size than in the species with weaker sexual selection.

Stepping off the pasture: evidence of widespread alternative male mating tactics in the yellow dung fly

Geoff Parker’s investigations of the yellow dung fly mating system revitalized interest in sexual selection theory, sparked development of sperm competition and sexual conflict theories, and stimulated use of this species as an important model system. Numerous studies across widespread populations have demonstrated large-male advantages in competition contests occurring on dung in cow pastures; however, recent work suggests that smaller males adopt an alternative mating tactic by avoiding dung and instead copulating with females at foraging sites. Though this finding has the potential to expand our understanding of sexual selection in yellow dung flies, such behavior has to date been documented at only one field site, raising the possibility that this phenomenon is highly localized. Here, we report the expression of size-dependent alternative mating tactics across three discrete populations. These findings provide a cautionary tale for researchers limiting their attention to aggregation sites where study organisms are most conveniently encountered.

Do male Trinidadian guppies adjust their alternative mating tactics in the presence of a rival male audience?

Males in polygamous mating systems may inadvertently transmit information regarding their mating preferences to bystanding sexual competitors, thereby permitting bystanders to use this information to enhance their own mating success by copying the mate choice of signallers. If males are at risk of having their mate choice copied and consequently face a higher risk of sexual competition, then selection should favour males that reduce conspicuous mating behaviours in the presence of an audience of sexual competitors. In the current study, we used the Trinidadian guppy (Poecilia reticulata), a species that exhibits alternative male mating tactics, to test this sexual competition avoidance hypothesis and the predictions that males would decrease their overall mating effort and exhibit fewer conspicuous courtship displays relative to more inconspicuous sneak mating attempts in the presence of either one or two sexual rivals compared to the absence of any audience. Male guppies significantly reduced their overall mating effort in the presence of increasing numbers of rival audience males. This was reflected in similar monotonic decreases in the frequencies of courtship displays and sneak mating attempts and in the proportional use of courtship displays (relative to sneak mating attempts) across treatments. These findings are consistent with the sexual competition avoidance hypothesis. Our novel results contribute to an increasing body of knowledge showing that the social environment can influence the mating effort and mating decisions of individuals and thus have important implications for sexual selection and evolution.

Exploring simultaneous allocation to mating effort, sperm production, and body growth in male guppies

In several species, males increase their mating and sperm investment in the presence of unfamiliar females, the so-called Coolidge effect. Such an elevated reproductive effort is expected to be associated with a decreased investment in other costly traits, such as somatic growth and maintenance. How precopulatory, postcopulatory, and somatic investments interact one with each other, however, has been rarely evaluated simultaneously. We used the guppy (Poecilia reticulata), a polyandrous livebearing fish with alternative male mating tactics, to compare these 3 investments between males whose encounter rate with unfamiliar females was experimentally maintained at either high (high mate encounter rate [HER]) or low rate (low mate encounter rate [LER]) for 4 months. At the end of this period, HER males showed an increased sperm production as compared with their LER counterparts. This increment was accompanied with a reduction in the time spent following the female and by a shift from costly courtship displays to gonopodial thrusting, a less expensive coercive mating tactic. This effect may indicate a trade-off between these 2 components of male reproductive investment or may reflect a change in male optimal reproductive strategy associated with different mate encounter rate. In contrast, body growth was positively correlated with the increase in sperm production, and did not differ between experimental groups. Collectively, these results suggest that males did not vary their overall reproductive investment in response to their encounter rate with unfamiliar females, but differed significantly in the amount of resources available individually.

Alternative male mating behaviour in the two-spotted spider mite: dependence on age and density

Alternative male mating tactics occur in many taxa, and usually include sneaking behaviour. Typically, sneaking behaviour is expressed by less competitive males to avoid fighting over females guarded by stronger males and to increase their mating chances, but in theory it can be expressed by any male as long as it improves his future reproduction. Recently, we characterized fighting and sneaking behaviour in males of the two-spotted spider mite that guard females during their preadult moulting stage. Sneaking behaviour involves not responding to rival males to avoid eliciting attack, whereas fighting behaviour involves challenging all rivals. To understand these alternative precopulatory behaviours from a life history perspective, we investigated (1) their heritability, and how they are affected by (2) male density, (3) male age and (4) competition between males differing in age. We established genetic lines for fighting or sneaking by crossing a male that displayed fighting or sneaking behaviour with one of his daughters. In fourth-generation males from these lines, however, the proportions of fighting and sneaking behaviour were not significantly different. The frequency of sneaking behaviour increased with male density, yet decreased with male age. Old males always displayed fighting and rarely lost females they guarded to young males, whereas young fighting males lost females to old rival males more frequently than young sneaking males. Of the young fighting males that did not lose the female they guarded to old males, about 40% switched to sneaking. We conclude that alternative male mating behaviours in this mite are not maintained as a genetic polymorphism, but arise from phenotypic plasticity in response to the male's environment (male density) and its own condition (age). We hypothesize that young males opt for sneaking behaviour because fighting jeopardises their future reproduction.

Integrative omics analysis reveals differentially distributed proteins in dimorphic euspermatozoa of the squid, Loligo bleekeri

In the coastal squid Loligo bleekeri, each male produces one of two types of fertilization-competent spermatozoa (eusperm) that exhibit morphological and behavioral differences. Large “consort” males produce short-tailed spermatozoa that display free-swimming behavior when ejaculated into seawater. Small “sneaker” males, on the other hand, produce long-tailed spermatozoa that exhibit a self-swarming trait after ejaculation. To understand the molecular basis for adaptive traits employed by alternative male mating tactics, we performed the transcriptome deep sequencing (RNA-seq) and proteome analyses to search for differences in testicular mRNAs and sperm proteins, respectively. From mature male testes we identified a total of 236,455 contigs (FPKM ≧1) where 3789 and 2789 were preferentially (≧10-fold) expressed in consort and sneaker testes, respectively. A proteomic analysis detected 4302 proteins in the mature sperm as post-translational products. A strongly biased (≧10-fold) distribution occurred in 55 consort proteins and 61 sneaker proteins. There was no clear mRNA–protein correlation, making a ballpark estimate impossible for not only overall protein abundance but also the degree of biased sperm type expressed in the spermatozoa. A family encoding dynein heavy chain gene, however, was found to be biased towards sneakers, whereas many enzymes involving energy metabolism were heavily biased towards consort spermatozoa. The difference in flagellar length matched exactly the different amount of tubulins. From these results we hypothesize that discrete differential traits in dimorphic eusperm arose from a series of innovative alterations in the intracellular components of spermatozoa.

Erratum to: The dynamics of alternative male mating tactics in a population of Black Grouse Tetrao tetrix in the Italian Alps

Erratum to: The dynamics of alternative male mating tactics in a population of Black Grouse Tetrao tetrix in the Italian Alps

Rutting behaviour of territorial and nonterritorial male chamois: Is there a home advantage?

Males using alternative male mating tactics (AMTs) may express their mating effort in a variety of ways. In polygynous species with limited sexual dimorphism, differences in male aggressiveness may affect mating opportunities. We recorded the behaviour of 8 territorial and 7 nonterritorial male Alpine chamois Rupicapra rupicapra, a nearly monomorphic ungulate, during the 2011 rut in the Gran Paradiso National Park (Italy), to analyse differences in mating effort and mating opportunities between AMTs. The chamois showed a rich behavioural repertoire (31 behavioural patterns), with a prevalence of indirect aggression. Territorial males had higher frequency of aggressive and courtship behaviour than nonterritorial males over the early rut. Later, nonterritorials increased their mating effort, possibly because of reduced competition with dominant males. Territorial males monopolised all observed mating events. Our results support the hypothesis that chamois may assert dominance through intense aggressiveness rather than through horn size or body mass as found in other polygynous ungulates. Most important, differences in mating effort mediated by AMTs resulted in different mating opportunities; these benefits, however, are traded off against greater costs, due to higher levels of hormone metabolites and parasitism. Data on AMTs flexibility, lifetime reproductive success and survival are needed to clarify the mechanisms underlying the evolution and maintenance of AMTs within chamois populations.

Male–male competition and alternative male mating tactics influence female behavior and fertility in Japanese medaka (Oryzias latipes)

Intense male–male competition driven by high male density during mating can result in the evolution of alternative mating tactics that increase male fertilization success. The effects of alternative male mating tactics on females can range from increased fertilization and genetic benefits to decreased fertilization and loss of paternal care. However, the influence of male competitive behavior and alternative mating tactics on female behavior and reproductive success has seldom been addressed. In this work, I investigated the occurrence of alternative male mating tactics and their potential influence on female behavior and fertilization success in Japanese medaka (Oryzias latipes). Groups of one, two, or four males competed for access to a female in a repeated-measures experiment. Male density had a significant influence on female reproductive output as a result of a change in competitive mode from contest to scramble competition that coincided with more disruption during mating when more than one male attempted to mate. By contrast, sneaking during mating was beneficial to males, as more than one male sired offspring in most spawnings involving sneaker males. These results suggest that there may be conflict between males and females over mating, such that females are detrimentally affected by the occurrence of alternative mating tactics, whereas males may benefit from sneak mating. The occurrence of conflict between the sexes can be related to ecological factors, such as male density, which cause behavioral change in both males and females.

Body size correlates with fertilization success but not gonad size in grass goby territorial males.

In fish species with alternative male mating tactics, sperm competition typically occurs when small males that are unsuccessful in direct contests steal fertilization opportunities from large dominant males. In the grass goby Zosterisessor ophiocephalus, large territorial males defend and court females from nest sites, while small sneaker males obtain matings by sneaking into nests. Parentage assignment of 688 eggs from 8 different nests sampled in the 2003–2004 breeding season revealed a high level of sperm competition. Fertilization success of territorial males was very high but in all nests sneakers also contributed to the progeny. In territorial males, fertilization success correlated positively with male body size. Gonadal investment was explored in a sample of 126 grass gobies collected during the period 1995–1996 in the same area (61 territorial males and 65 sneakers). Correlation between body weight and testis weight was positive and significant for sneaker males, while correlation was virtually equal to zero in territorial males. That body size in territorial males is correlated with fertilization success but not gonad size suggests that males allocate much more energy into growth and relatively little into sperm production once the needed size to become territorial is attained. The increased paternity of larger territorial males might be due to a more effective defense of the nest in comparison with smaller territorial males.

The dynamics of alternative male mating tactics in a population of Black Grouse Tetrao tetrix in the Italian Alps

The Black Grouse Tetrao tetrix is primarily a lekking species, although in some populations solitary display is also common. We analysed data from a 25-year-long survey of an increasing Black Grouse population in the western Italian Alps in order to test whether the numbers of males adopting different tactics conformed to patterns expected, based on the hypothesis that dominant birds occupy the leks and solitary displaying birds are subordinate, and that the tendency for birds to be excluded from leks increases with lek size. Four predictions were made to test this hypothesis: (1) the proportion of solitary males would increase as the overall population increases, (2) there would be a threshold at which there is little or no increase in the size of the lekking population, but continued increase in the population of solitary displaying birds, (3) available lek habitat would be occupied prior to an increase in solitary displaying males, and (4) there would be an increase in the use of less preferred habitat by solitary displaying males as the total population increases. Population trends varied according to display status, in that the lekking population reached an apparent threshold while the number of solitary males continued to increase, and there was an expansion of the range of solitary males into higher altitudes in years when the population was larger. However, there was no increase in the proportion of solitary males as the total population increased. Furthermore, there was no suggestion that suitable lek habitat was limiting, as the number of leks and the mean size of those leks continued to increase throughout the study period. Although two predictions were supported, the precise patterns of trends, and results of additional analyses, suggested that solitary display is more likely to be an alternative rather than a subordinate tactic. Several factors may promote this apparent dual display tactic in Black Grouse, but habitat structure in this and other Alpine populations is likely to be a key influence.

Queuing in space and time reduces the lek paradox on an antelope lek

Lek systems, where females often use centrality to assess male quality, highlight a general paradox in evolutionary biology: how can female preferences for males providing good genes persist when consequential strong directional selection is predicted to deplete additive genetic variance in male quality and thereby obliterate benefits of choosiness? An explanation contributing to the resolution of this lek paradox may be that genetic variance is retained when an indirect mate choice cue, such as centrality on a lek, is an imperfect indicator of male genetic quality. Here I investigate whether the presence of alternative male mating tactics limits the reliability of centrality as a quality indicator in lek-breeding topi antelopes. Whereas males establishing territories directly on the central lek were relatively large, smaller peripheral males regularly shifted their territories centripetally and in this way also occasionally obtained central territories. By such opportunistic queuing, small males could increase their mating success drastically; however, their territorial tenure in the lek centre was relatively short, consistent with moderate competitive ability. These results suggest that male topi antelopes can obtain central lek territories through alternative mating tactics, providing scope for variance in male quality on the central lek. In a separate finding, the mating success of central males was found to increase during territorial tenure, independent of estimated age. The demonstration of queuing in both space and time on a mammalian lek highlights the importance of considering male tactical dynamics over time in order to avoid an inflated appearance of the lek paradox.