Polyandry and alternative mating tactics

Many species in the animal kingdom are characterized by alternative mating tactics (AMTs) within a sex. In males, such tactics include mate guarding versus sneaking behaviours, or territorial versus female mimicry. Although AMTs can occur in either sex, they have been most commonly described in males. This sex bias may, in part, reflect the increased opportunity for sexual selection that typically exists in males, which can result in a higher probability that AMTs evolve in that sex. Consequently, females and polyandry can play a pivotal role in governing the reproductive success associated with male AMTs and in the evolutionary dynamics of the tactics. In this review, we discuss polyandry and the evolution of AMTs. First, we define AMTs and review game theoretical and quantitative genetic approaches used to model their evolution. Second, we review several examples of AMTs, highlighting the roles that genes and environment play in phenotype expression and development of the tactics, as well as empirical approaches to differentiating among the mechanisms. Third, ecological and genetic constraints to the evolution of AMTs are discussed. Fourth, we speculate on why female AMTs are less reported on in the literature than male tactics. Fifth, we examine the effects of AMTs on breeding outcomes and female fitness, and as a source, and possibly also a consequence, of sexual conflict. We conclude by suggesting a new model for the evolution of AMTs that incorporates both environmental and genetic effects, and discuss some future avenues of research.     

Size-dependent alternative male mating tactics in the yellow dung fly,Scathophaga stercoraria

Whenever males can monopolize females and/or resources used by females, the opportunity for sexual selection will be great. The greater the variation among males in reproductive success, the greater the intensity of selection on less competitive males to gain matings through alternative tactics. In the yellow dung fly, Scathophaga stercoraria, males aggressively compete for access to receptive, gravid females on fresh dung. Larger males are better able to acquire mates and to complete copulation successfully and guard the female throughout oviposition. Here we demonstrate that when an alternative resource is present where females aggregate (i.e. apple pomace, where both sexes come to feed), smaller males will redirect their searching for females from dung to the new substrate. In addition, we identify a class of particularly small males on the alternative substrate that appears never to be present searching for females on or around dung. Smaller males were found to have a mating ‘advantage’ on pomace, in striking contrast to the pattern observed on dung, providing further support for the existence of an alternative male reproductive tactic in this species.     

Insemination efficiency of two alternative male mating tactics in the guppy Poecilia reticulata

In this study we compared the insemination efficiency of two alternative mating tactics (courtship and sneak mating) in the guppy Poecilia reticulata by quantifying the number of sperm delivered during a copulation. During a single copulation, guppies delivered between zero and 92% of the sperm available, as determined by mechanically stripping the males'' sperm reserve at rest. The absolute number of sperm delivered after courtship was three times larger than that delivered through sneak mating; nonetheless, the variance was large with both tactics and the two distributions largely overlapped. The number of sperm available at rest increased with male size. With both tactics, the number of sperm delivered was positively correlated with the sperm available. Contrary to courtship copulations, in sneak copulations there was no correlation between the number of sperm delivered and male size. However, once the data were standardized for sperm reserve, small males delivered a larger proportion of their available sperm during sneak copulation. The rate of sexual acts (sigmoid and thrust rate) before copulation was not correlated with the number of sperm available. After the occurrence of a copulation in both the courtship and sneak copulation groups, the sexual activity of the male decreased in proportion to the amount of sperm he previously inseminated.     

Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata)

In the guppy (Poecilia reticulata), males have two alternative mating tactics. Individual males may either display to a receptive female prior to attempting to copulate with her or attempt to quickly sneakcopulate with a female without first displaying to her or without a prior receptive response from her. In this study, I experimentally investigated the effects of simulated local increases in the risk of predation (in the form of a cichlid fish predator model in situ) on the mating tactics used by free-ranging male guppies in two typical macrohabitats (riffle and pool) of a Trinidadian river. Focal male guppies displayed to females significantly less often on average, and conversely attempted sneak copulations more often, in the presence of the predator model than in its absence; this pattern was similar for both habitats. These fish therefore performed a lower proportion of sigmoid displays and increased their sneaky mating attempts when the apparent risk of predation had increased locally. This predator-mediated response is consistent with a trade-off between mating success and risk of mortality due to predation. The results are the first to confirm risk-sensitive mating behaviour in free-ranging male guppies within a population, and demonstrate the potential importance of predators in influencing the relative use of alternative mating tactics in this species on a microgeographical scale in the wild.     

Alternative male mating tactics in Gobius niger

In the field, parental males of the black goby Gobius niger were always >9 cm L _T, showed a conspicuous elongation of the first dorsal fin, and were darkly coloured. Larger parental males did not occupy larger nests or obtain more eggs, suggesting that over a threshold size reproductive success was not correlated with male size. The mating system was polygynous with different egg clutches simultaneously present in a nest. Smaller sexually mature males were observed around and inside nests in which spawning was occurring. These opportunistic males ranged in body size between 6 to 8 cm L _T. In contrast to parental males, they did not show an exaggeration of the first dorsal fin and were cryptically coloured, thus resembling small females in their external morphology. Aquarium experiments confirmed that smaller males perform a sneaking behaviour, releasing sperm when parental males spawn. As a consequence, it is possible to define three male types: type I are small, without an elongated dorsal fin and adopt a sneaking mating tactic; type III are large, have a pronounced elongation of the dorsal fin and perform parental behaviour; type II are intermediate both in size and elongation of the first dorsal fin and behave as either as sneakers or, possibly, as parental males according to nest availability and male competition.     

Wing length and asymmetry of male Tokunagayusurika akamusi chironomid midges using alternative mating tactics

Male Tokunagayusurika akamusi chironomids have alternative mating tactics.One is to search for females on vegetation (ground mating),and the other is to wait for females in an aerial swarm (swarmmating). Simultaneous sampling of ground-unpaired and ground-pairedmales and of swarm-unpaired and swarm-paired males were performed.The average wing length and right-left wing length difference(wing asymmetry) were compared between males from the four differentcategories. Swarm-unpaired males were larger than ground-unpaired ones,swarm-paired males were larger than swarm-unpaired ones, and ground-pairedmales were not larger than ground-unpaired ones. Thus, large malestended to aggregate in swarms, and larger swarming males matedmore successfully. On the other hand, small males probably enjoyedmating on the ground, especially when large males swarmed. Thewing asymmetry was not significantly different between unpairedand paired males both within and between tactics. There wasa flat or U-shaped relationship between wing length and asymmetry,underpinning the lack of a symmetrical advantage of swarmingto large males. The right-left difference was not normally distributedin four of six samples of unpaired males but, in contrast, wasnot normally distributed in only one of six samples of pairedmales. The non-normal distributions were leptokurtic and includedoutliers. Removal of the outliers improved normality, suggestingthat males with extremely asymmetric wings were not successfulin mating.     

Female mate assessment and choice behavior affect the frequency of alternative male mating tactics

Explanations for the existence of alternative male mating tacticsfocus primarily on male–male competition. Mating systems,however, are composed of interactions both within and betweenthe sexes, and the role of female behavior in shaping male matingtactics should not be overlooked. By using a dynamic state variablegame model, I examine how female mate assessment and choicebehavior affect the frequency of alternative male mating tactics.When females can accurately assess the quality of males, onlymales with high quality are likely to be chosen as mates, andthus, lower-quality males gain little fitness from courtingfemales. This leads lower-quality males to switch to an alternativemating tactic that attempts to circumvent female mate choice.In contrast, if the abilities of females to accurately assessmales are constrained by assessment costs, imperfect information,or time constraints, or if the pool of available males is smaller,then lower-quality males are increasingly chosen as mates andthey less often use alternative mating tactics. Thus, femalebehavior shapes the frequency of alternative male mating tactics.A consequence of this game between the sexes is that male behavior(i.e., increased alternative mating tactics) decreases the benefitsfemales might otherwise gain from lower assessment costs, clearersignals of male quality, more time to choose a male, and moremales from which to choose a mate.     

Variability of GnRH secretion in two goby species with socially controlled alternative male mating tactics

Male reproductive phenotypic plasticity related to environmental-social conditions is common among teleost fish. In several species, males adopt different mating tactics depending on their size, monopolizing mates when larger, while parasitizing dominant male spawns when smaller. Males performing alternative mating tactics are often characterized by a strong dimorphism in both primary and secondary reproductive traits. According to studies on sex-changing species and on species where only one male morph is reproductively active, male alternative phenotypes are expected to vary also in gonadotropin-releasing hormone (GnRH) neurons in forebrain preoptic area (POA). Here, we compared the intra- and inter-sexual variations in number and size of GnRH neurons, along with gonads and male accessory structure investment, in two goby species, the grass goby, Zosterisessor ophiocephalus, and the black goby, Gobius niger, characterized by male alternative mating phenotypes. In both species, older and larger males defend nests, court and perform parental care, while younger and smaller ones try to sneak territorial male spawning. We found that grass goby and black goby have different patterns of GnRH expression. Grass goby presents a clear intra-sexual dimorphism in GnRH expression, related to the occurrence of alternative mating tactics, while in the black goby, only inter-sexual differences are observed. The inter- and intra-specific variability in the GnRH neurons in these two goby species is discussed in light of the differences in migratory behavior, nest type, and mating system.     

Male trait distribution determined alternative mating tactics in guppies

The distribution of the percentage of the body of male guppies Poecilia reticulata covered with orange coloration influenced alternative mating tactics. At 15% mean coverage, male guppies interfered with other courting males more and engaged in courtship activities longer than males with 10% mean coverage. When males were tested in a situation with a wide variety of male types, males switched among females less frequently than when the variance among males was low.     

Seasonal variation in male alternative reproductive tactics

Genetic parentage analyses reveal considerable diversity in alternative reproductive behaviours (e.g. sneaking) in many taxa. However, little is known about whether these behaviours vary seasonally and between populations. Here, we investigate seasonal variation in male reproductive behaviours in a population of two‐spotted gobies (Gobiusculus flavescens) in Norway. Male two‐spotted gobies guard nests, attract females and care for fertilized eggs. We collected clutches and nest‐guarding males early and late in the breeding season in artificial nests and used microsatellite markers to reconstruct parentage from a subset of offspring from each nest. We hypothesized that mating, reproductive success and sneaking should be more prevalent early in the breeding season when competition for mates among males is predicted to be higher. However, parentage analyses revealed similar values of mating, reproductive success and high frequencies of successful sneaking early (30% of nests) and late (27% of nests) in the season. We also found that multiple females with eggs in the same nest were fertilized by one or more sneaker males, indicating that some males in this population engage in a satellite strategy. We contrast our results to previous work that demonstrates low levels of cuckoldry in a population in Sweden. Our results demonstrate marked stability in both the genetic mating system and male alternative reproductive tactics over the breeding season. However, sneaking rates may vary geographically within a species, likely due to local selection influencing ecological factors encountered at different locations.     

Vocalizations of bearded seals (Erignathus barbatus) and their influence on the soundscape of the western Canadian Arctic

The soundscape is a crucial habitat feature for marine mammals. This study investigates the contribution of bearded seal vocalizations to the soundscape in the western Canadian Arctic, and also the vocal characteristics of bearded seals relative to sea ice conditions. Passive acoustic data were recorded near Sachs Harbour between August 2015 and July 2016. Sound pressure levels (SPL) in the 50–1,000 Hz and 1–10 kHz bands increased as the total duration of all bearded seal vocalizations increased, and this relationship was moderated by sea ice concentration. Bearded seals in this region had an overlapping vocal repertoire with bearded seals in other areas of the Arctic, and had seven additional vocalizations that have not been previously documented for this region. This study is the first detailed assessment of the influence of bearded seal calls on SPL, which shows the high potential of bearded seals to influence underwater sound levels during the mating season. Bearded seals live in a changing Arctic seascape, and their influence on the soundscape may shift as sea ice continues to diminish. It is imperative that acoustic monitoring continues within the Arctic, and this study provides a baseline for future monitoring as the Arctic continues to change.     

Alternative mating tactics and extreme male dimorphism in fig wasps

The dimorphisms in morphology and behaviour of male fig wasps are among the most extreme in the animal kingdom, and offer excellent opportunities to test the predictions of certain sexual selection models. Winged males resemble their conspecific females closely, but wingless males are so divergent in form that they have repeatedly been classified into different taxa. Wingless males mate within their natal fig fruits, whereas winged males disperse to mate. Individual species may have winged males, wingless males or both morphs. A key hypothesis proposes that sexual selection on male mating opportunities favours winged males in species with small broods and wingless males in species with large broods. Using data from 114 species in 33 genera, we show that both simple and formal comparative analyses support the correlated evolution of large brood size and male winglessness. Theoretical models further predict that, in male dimorphic species, the proportion of winged males should equal (in cases without local mate competition) or exceed (in cases with local mate competition) the proportion of females developing in fig fruits without wingless males. These predictions are met by eight out of nine male dimorphic species studied. Taken together, the patterns across all species, and between different male dimorphic species, strongly support sexual selection on mating opportunities as the major determinant of male morph ratios in fig wasps.     

Environmental heterogeneity and alternative mating tactics in the damselfly Protoneura amatoria

Conditional male mating strategies have been studied extensivelyin relation to male attributes, such as size and resource-holdingpotential, but few studies have considered the effects of environmentalheterogeneity on the use of alternative mating tactics. In somesystems, environmental heterogeneity may be the key to understandingthe evolution and maintenance of such polyphenisms. I examinedthe influence of the physical environment on the use of alternativetactics by the damselfly Protoneura amatoria. Male P. amatoriareversibly use 2 tactics to gain matings: 1) sit and wait inthe canopy for passing females or 2) hover over the water andattempt to grab females that are ovipositing in floating debris.Observations in 3 streams indicated that the use of the hoveringtactic was greater under high-light than low-light conditionsand at higher densities of ovipositing females. The densityof ovipositing females was correlated with both the light conditionsand the availability of oviposition substrate, indicating thatphysical factors exert indirect as well as direct influenceson tactic use. Experimental manipulations showed that both malesand females responded directly to light conditions and suggestedthat males responded directly to the density of ovipositingfemales. These results can be explained largely in terms ofthe cues and constraints inherent in different light environments.Thus, the conditional mating strategy of P. amatoria appearsto have evolved in response to, and been maintained by, fine-scalevariation in the physical environment. These findings are discussedin relation to flight dynamics and predation risk.     

Resource availability,mating opportunity and sexual selection intensity influence the expression of male alternative reproductive tactics

The expression of alternative reproductive tactics can be plastic and occur simultaneously depending on cues that vary spatially or temporally. For example, variation in resources and sexual selection intensity is expected to influence the pay‐off of each tactic and shape the decision of which tactic to employ. Males of the nuptial gift‐giving spider Pisaura mirabilis can adopt three tactics: offering a genuine prey gift, a ‘worthless’ non‐nutritious gift or no gift. We hypothesized that resources and/or male body condition, and mating opportunity and sexual selection intensity, vary over the course of the mating season to shape the co‐existence of alternative traits. We measured these variables in the field over two seasons, to investigate the predictions that as the mating season progresses, (i) males become more likely to employ a gift‐giving tactic, and (ii) the likelihood of switching from worthless to genuine gifts increases. Prey availability increased over the season and co‐varied with the propensity of males to employ the gift‐giving tactic, but we found no support for condition‐dependent gift giving. Males responded to an increase in female availability by increasing their mating effort (gift production). Furthermore, the frequency of genuine gift use increased with sexual selection intensity, consistent with the assumption that sperm competition intensity increases with time. Our results suggest that the frequency of alternative tactics is shaped by seasonal changes in ecological factors and sexual selection. This leads to relaxed selection for the gift‐giving tactic early in the season when females are less choosy and resources more scarce, and increased selection for genuine gifts later in the season driven by mating opportunity and risk of sperm competition.     

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.