Evolution Of Alternative Mating Tactics Research Articles

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.

A mating plug in a squid? Sneaker spermatophores can block the female sperm-storage organ in Doryteuthis plei

Males from numerous animal taxa have evolved strategies for obstructing the female genitalia with copulatory plugs, reducing the risk of sperm competition and thus resulting in an advantage in sexual selection. Several lines of evidence suggest that sperm competition is a common feature in the complex squid mating systems, which include the evolution of alternative mating tactics (consort vs. sneaker). However, mating plugs have hitherto not been reported for the group. Investigating the female sperm-storage organ (i.e., seminal receptacle, SR) of the squid Doryteuthis plei, we found cases in which everted spermatophores (i.e., spermatangia) were implanted into the SR and blocking its opening. Here, we describe this finding of “plugged spermatangia” based on microscopy analyses (histology and microCT) of SRs of females from three experimental groups (before and after recent mating and after egg release). We show that sneaker male spermatophores may block the opening of the SR, possibly functioning as temporary copulatory plugs that physically obstruct the SR. Together with previous experimental data on spermatophore functioning, our results suggest that plug efficiency is high until at least 5 h after mating, when spermatangia are turgid and full of sperm, clogging the organ’s opening. After that time, plugs gradually decrease their efficiency as they lose turgidity by releasing part of their sperm content. However, one experimental female still had a plugged spermatangium blocking a major portion of the opening even after 48 h without mating. Within the context of squid mating systems and sexual selection, we hypothesize that plugged spermatangia are a sneaker strategy associated with minimizing sperm competition between sneaker males.

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.

Density affects mating mode and large male mating advantage in a fiddler crab

Fiddler crabs show two different mating modes: either females search and crabs mate underground in male burrows, or males search and crabs mate on the surface near female burrows. We explored the relationship between crab density, body size, the searching behavior of both sexes, and the occurrence of both mating modes in the fiddler crab Uca uruguayensis. We found that crabs change their mating mode depending on their size and crab density. Crabs mated mostly on the surface at low densities, and underground at high densities. The proportion of wandering receptive females but not courting males accounted for the variation in mating modes. This suggests that whether crabs mate underground (or on the surface) is determined by the presence (or absence) of searching females. We found that the change in the mating mode affected the level of assortative mating; males mating underground were bigger than those mating on the surface, suggesting active female choice. Given that fiddler crabs experience multiple reproductive cycles, they are prone to showing behavioral plasticity in their mating strategy whenever the payoffs of using different mating modes differ between reproductive events. Our results suggest that the incorporation of different levels of environmental variability may be important in theoretical models aimed at improving our understanding of the evolution of alternative mating tactics and strategies.

Effects of timing of nest entry and body size on the fertilization success of alternative male reproductive phenotypes of masu salmon (Oncorhynchus masou)

Using a natural population of masu salmon ( Oncorhynchus masou (Brevoort, 1856)) in a stream of Shikaribetsu Lake, Hokkaido, Japan, we combined behavioural observations with genetic parentage analysis to explore the factors affecting fertilization success achieved by alternative mating tactics (fighting by large migratory males and sneaking by small mature male parr). Larger males gained priority access to females; migrant males do this by holding a guarding position near the nesting female and mature male parr do this by adopting sneaker behaviour and attending spawning groups. Status of mature male parr was related to success of nest entry but not to timing of nest entry, although the timing of nest entry influenced fertilization success of sneakers and ejaculation simultaneous with pair spawning was needed for fertilization by sneakers. The relative body size of each male who successfully spawned with a female is also likely to determine the proportion of eggs he fertilized because larger males have larger ejaculate. These results provide insight into factors relating to variation in fertilization success, how body size dimorphisms may be related to fitness, and evolution of alternative mating tactics.

Mating tactics of male feral goats (Capra hircus): risks and benefits

Intense competition between males for reproduction has led to the evolution of alternative mating tactics (AMTs). Feral goat males usually use a tactic called tending, in which they defend oestrous females from other males. Males may also use a second mating tactic called coursing, in which they gain access to oestrous females by disturbing a tending pair. Herein, we examine estimated mating success (EMS) and risks of using these tactics. Tending was only used by mature (≥4 years old), higher-ranking males and accounted for 75% of EMS. Coursing was used by males of all ages and dominance ranks, and accounted for 25% of EMS. Using coursing, male kids achieved 8% of EMS. Mature males achieved 92% of EMS. Both age and dominance rank were related to EMS, but age was not important after its relationship with dominance was controlled. Tending bouts were, on average, ca. 30 min long, while coursing bouts only averaged ca. 2 min. Males were more likely to suffer a butt while coursing than while tending, and formerly tending males were responsible for most butts. Kids that coursed had the highest risk of being butted. In most AMTs, there are reductions in the risks in relation to low fitness benefits. However, we found that the risks of butts during coursing were high, while our evidence suggests that the EMS was probably low. Nevertheless, the existence of an effective AMT in male feral goats may have an important influence on the intensity of sexual selection and the effective population size.

Condition-dependent sexual traits and social dominance in the house finch

Elaboration of costly sexual traits can reduce investment in other aspects of reproduction, such as parental care or intrasexual competition, which may lead to the evolution of alternative mating tactics. In house finches (Carpodacus mexicanus), less elaborately ornamented (dull) males tend to dominate more elaborated (redder) males, but redder males pair earlier and invest more in parental care. This suggests that males may pursue alternative parental or competitive tactics, depending on the elaboration of their sexual trait. Elevation of testosterone, a hormone that is closely associated with condition in male house finches, influences dominance and sexual behaviors but is antagonistic to parental behaviors. We tested the hypothesis that the higher dominance status of dull males reflects an alternative testosterone-dependent mating tactic. First, we experimentally manipulated the testosterone levels of captive males and measured the effect on dominance rank, and second, we measured the association of testosterone elevation and plumage hue in free-living males. We found that, as predicted, testosterone elevation increased dominance rank in captive males. However, in free-living males, testosterone levels were higher in redder males, suggesting that testosterone is dissociated from dominance status under natural circumstances. This may be because the context of social interactions and the higher motivation of dull males to access food resources have a stronger influence on the outcome of dominance interactions than does the physiological effects of testosterone elevation. In turn, the strong positive correlation between testosterone levels and plumage elaboration likely reflects the common condition dependence of these traits. Key words: condition-dependent, house finch, sexual ornament, testosterone. [Behav Ecol 15:779–784 (2004)]

Evolution of alternative mating tactics: conditional versus mixed strategies

Intrasexual polymorphisms have evolved in a wide range of organisms. Most of them have been interpreted as the product of conditional strategies in which the tactic an individual adopts is determined by some aspect of state (e.g., age, size, condition). However, there are a few examples that appear to represent an evolutionarily stable mixture of heritable pure strategies that are maintained by frequency-dependent selection. In the present study, we produce a model of a mating system with two morphs: a territorial morph and a sneak morph. By varying the costs and limits associated with conditional strategies, mating skew, and the proportion of matings obtained by sneaking males, we examine the conditions that favor the evolution of conditional versus pure strategies. Contrary to current thinking, our results show that as long as either costs or limits are greater than zero, conditional strategists are never able to entirely replace pure strategists, and equilibrium populations may frequently consist of a mixture of conditional and pure strategists. Our results suggest that conditional strategists will be most frequent at intermediate levels of mating skew. Polymorphisms in which conditional strategists are rare or absent are most likely to evolve when mating skew is extremely high, the costs and limits of plasticity are very high, or the benefits of being conditional are very low. The limited data available suggest that high mating skew is probably the most important factor. Key words: alternative strategies, conditional strategies, costs of plasticity, mating competition, mating skew, polymorphism, tactics. [Behav Ecol 15:534–542 (2004)]

Increased performance of offspring sired by parasitic males in bluegill sunfish

Males of many species are characterized by alternative mating tactics. In bluegill sunfish (Lepomis macrochirus), some males delay maturation and become ‘‘parentals’’ while other males mature precociously and become ‘‘cuckolders.’’ Parentals use an overt, territorial mating tactic, defending a nest and courting females. Cuckolders instead use a sneaking tactic to parasitize parentals. It has previously been shown that parentals that are heavily cuckolded provide less care to their young, yet females do not appear to discriminate against cuckolders, and they may actually release more eggs when a cuckolder is present than when spawning only with a parental. Here I examined growth rate of fry of known paternity through the yolk-sac stage of development using complementary laboratory and field studies to assess a potential indirect benefit for females that mate with cuckolders. Comparison of maternal half-siblings sired in vitro shows that cuckolder offspring grow faster and to a larger size than parental offspring while feeding endogenously on their yolk sac. Because both food resource and maternal genes are equivalent across treatments, these data indicate a genetic difference in growth between the two male life histories. In the field, fry from nests that have proportionately more cuckolder offspring are larger when they emerge from the nest. This increased size can lead to threefold higher survivorship for cuckolder offspring than parental offspring from Hydra canadensis predation, a major predator of bluegill fry. These results are discussed in the context of mate choice for direct and indirect benefits and in the context of the evolution of alternative mating tactics. Key words: bluegill sunfish, good genes, growth rate, indirect benefits, Lepomis macrochirus, mate choice, mating systems. [Behav Ecol 15:327–331 (2004)]

Maternal control of offspring sex and male morphology in the Otitesella fig wasps

Models concerning the evolution of alternative mating tactics commonly assume that individuals determine their own strategies. Here we develop a computer-based ESS model that allows mothers, ovipositing in discrete patches, to choose both the sex and the male mating tactics (natal-patch mating or dispersing) of their offspring based only on how many other mothers have used the specific patch before them. Data for three species of nonpollinating fig wasps from the Otitesella genus agree quantitatively with the model's assumptions and predictions. This suggests that females respond to population densities at the level of individual figs. The alternative male tactics in the species we studied are probably a result of a conditional strategy exercised by the mother that laid them. In addition, as females were only allowed to lay one egg per patch, our results suggest a new mechanism that can skew population sex ratios towards a female bias.

The evolution of alternative cryptic female choice strategies in age-structured populations.

Cryptic female choice is a potentially important aspect of the sexual selection process. According to the theory of sexual dialectics, postcopulation manipulation of relative male fertilization success can provide an avenue by which females can circumvent attempts by males to control female reproduction. Here I use stochastic models to investigate the evolution of cryptic female choice in populations with and without age structure. In populations without age structure, cryptic female choice will evolve only when (1) precopulatory mate choice by females is inefficient, (2) variation in male fitness is correlated with a trait upon which a female can base her choice of mates, and (3) the cost of multiple mating is not too high. In populations with age structure, similar conditions apply. However, selection sometimes favors females that employ alternative strategies of female choice at different ages. These results help to define the types of biological systems in which we should expect to see the evolution of cryptic female choice. They also illustrate that the evolution of choice strategies in females may be complex and may mirror in some important respects the evolution of alternative mating tactics in males.

Investigating the consistency of mate-locating behavior in the territorial butterfly Hypolimnas bolina (Lepidoptera : Nymphalidae)

The study of butterfly behavior has afforded valuable insights into the evolution of alternative mating tactics. Two hypotheses derived from this area of research contend that (1) territoriality is only viable under low to moderate conspecific densities (due to the costs of site defence) and (2) perching may be employed only when thermal conditions constrain flight activity. These hypotheses were evaluated by investigating mate locating behavior in Hypolimnas bolina, a territorial species that is naturally subject to variation in population density and weather conditions. Male behavior was charted throughout the day during a period of high population density at an encounter site in tropical Australia. Perching was the primary tactic, although a small proportion of individuals patrolled nonaggressively in the afternoon. Population-level male behavior failed to support predictions drawn from either the “territory economics” or “thermal constraint” hypotheses. First, the proportion of perching males and the number of aggressive conspecific interactions (per male) increased with increasing male density at the site. Second, few males patrolled at the hottest, brightest time of day (approximately midday), and the diel distribution of perchers did not emulate the “U-shaped” distribution shown by the occurrence of dorsal basking behavior. These results show that perching in this species is not a suboptimal tactic employed when temperatures constrain flight activity but may represent the best method of locating receptive females. At this stage the reproductive significance of the observed patrolling behavior remains obscure.

On Alternative Reproductive Tactics in Anurans: Dynamic Games with Density and Frequency Dependence

Intense mating competition and mate choice has favored the evolution of alternative mating tactics in many species. We developed a stochastic dynamic game to evaluate the choice among three alternative mating tactics by male anurans: call, satellite, or leave the chorus to forage or hide. The strategies were assumed to differ in mating success (call > satellite forage = hide), predation risk (call > satellite > forage > hide), and energetic expense (call > satellite = hide > forage). Six major predictions were derived. First, in relatively stable environments, males should enter a chorus in a synchronous pulsed pattern, with first-year males primarily choosing to be satellites on older calling males. The pulsed pattern is caused by the relatively high energetic cost of calling and the dependence of female arrival rates on chorus size (which promotes synchronization). In unstable environments, energetic constraints are reduced because favorable conditions are rare, so most males should call on favorable ni...