Alternative Reproductive Tactics in Context: How Demography, Ecology, and Behavior Affect Male Mating Success.

Alternative reproductive tactics may arise when natural enemies use sexual signals to locate the signaler. In field crickets, elevated costs to male calling due to acoustically orienting parasitoid flies create opportunity for an alternative tactic, satellite behavior, where noncalling males intercept females attracted to callers. Although the caller-satellite system in crickets that risk detection by parasitoids resembles distinct behavioral phenotypes, a male's propensity to behave as caller or satellite can be a continuously variable trait over several temporal scales, and an individual may pursue alternate tactics at different times. We modeled a caller-satellite-parasitoid system as a spatially explicit interaction among male and female crickets using individual-based simulation. Males varied in their propensity to call versus behave as a satellite from one night to the next. We varied mortality, density, sex ratio, and female mating behavior, and recorded lifetime number of mates as a function of a male's probability of calling (vs. acting as a satellite) along a gradient in parasitism risk. Frequently, the optimal behavior switched abruptly from being pure caller (call every night) to pure satellite (never call) as parasitism rate increased. However, mixed strategies prevailed even with high parasitism risk under conditions of higher background mortality rate, decreasing density, increasing female-biased sex ratio, and increasing female choosiness. In natural populations, high parasitoid pressure alone would be unlikely to yield fixation of pure satellite behavior.

Simulation of alternative male reproductive behavior: calling and satellite behavior in field crickets

Alternative reproductive tactics (ARTs) represent distinct behavioural phenotypes to maximize reproductive success within the same sex, primarily males, and may be genetically and/or conditionally determined. Across animals, intragenerational determinants of conditional ARTs are relatively well understood but transgenerational (non‐genetic) effects of parental ARTs on filial ARTs are largely unknown. Here, we assessed parental effects of conditional male ARTs on sons' ARTs in arrhenotokous spider mites Tetranychus urticae. Arrhenotoky, that is, males arising from unfertilized and females from fertilized eggs, sets the stage for sexual and transgenerational conflicts between male mates and females and their sons. Male ARTs of T. urticae are dichotomous, fighting and sneaking, and apparent in male–male combat and pre‐copulatory guarding behaviour. Due to haplodiploidy, male ARTs can only exert non‐genetic effects on sons of their mates. We hypothesized that parental ART effects are likely to occur in T. urticae because maternal ART mating status (unmated, sneaker‐ or fighter‐mated) is indicative of the offspring' social environment and ART flexibility rather prevails in younger than older males. Fighter‐mated mothers produced more offspring than unmated mothers and had a more daughter‐biased offspring sex ratio than unmated and sneaker‐mated mothers. Sons of fighter‐mated mothers were more likely to guard and did so earlier than sons of unmated and sneaker‐mated mothers. Unmated and sneaker‐mated, but not fighter‐mated, mothers produced sneaker sons that were quicker to start guarding than were fighter sons. Proximately, parental ART effects on sons' ARTs were most likely mediated by differences in seminal fluids. Ultimately, observed alterations of sons' ARTs represent adaptive maternal responses to ART phenotypes rather than manipulation by male mates. Fighter‐mated mothers tuned filial ARTs to male‐competitive environments whereas unmated and sneaker‐mated mothers tuned them to benign environments. Observed alterations in reproductive traits of fighter‐mated mothers suggest adaptive manipulation by the fighter phenotype or aligned male and female interests. Overall, our study documents previously unknown transgenerational ART effects on haploid sons' ARTs. A free Plain Language Summary can be found within the Supporting Information of this article.

Almost all life on earth is facing environmental change, and understanding how populations will respond to these changes is of urgent importance. One factor that is known to affect the speed by which a population can evolve when faced with changes in the environment is strong sexual selection. This increases the adaptive capacity of a population by increasing reproductive skew toward well-adapted (usually) males who will, on average, be best able to compete for matings. This effect could potentially be disrupted when males pursue alternative reproductive tactics (ARTs), whereby males within a species exhibit qualitatively different behaviors in their pursuit of matings. ARTs are diverse, but one common class is those expressed through condition-dependent polyphenism such that high-quality, well-adapted males compete aggressively for mates and low-quality, poorly adapted males attempt to acquire matings via other, nonaggressive behaviors. Here, using an individual-based modeling approach, we consider the possible impacts of ARTs on adaptation and evolutionary rescue. When the ART is simultaneous, meaning that low-quality males not only engage in contests but also pursue other tactics, adaptive capacity is reduced and evolutionary rescue, where a population avoids extinction by adapting to a changing environment, becomes less likely. This is because the use of the ART allows low-quality males to contribute more maladaptive genes to the population than would happen otherwise. When the ART is fixed, however, such that low-quality males will only use the alternative tactic and do not engage in contests, we find the opposite: adaptation happens more quickly and evolutionary rescue when the environment changes is more likely. This surprising effect is caused by an increase in the mating success of the highest quality males who face many fewer competitors in this scenario-counterintuitively, the presence of males pursuing the ART increases reproductive skew toward those males in the best condition.

In this study I examined the relationship among abundance of reproductive resources, population density, and adult sex ratio in the strawberry dart-poison frog, Dendrobates pumilio, and how these variables in turn influence the mating system, male reproductive success, and sexual selection. I studied the mating behavior in two populations of D. pumilio living in a primary and secondary rainforest on the Caribbean slope of Costa Rica. The abundance of tadpole-rearing sites (reproductive resources for females) was approximately 10-fold higher in the secondary forest. Accordingly, the population density was higher and the adult sex ratio was strongly female biased in the secondary forest, whereas the adult sex ratio was even in the primary forest. The female-biased sex ratio was associated with a higher level of polygyny and higher male mating and reproductive success in the secondary forest. In contrast, the level of polyandry did not differ between habitats. As expected, the opportunity for sexual selection on male mating success was lower in the secondary forest, the habitat with high female density. In conclusion, my results suggest that ecological variables such as resource availability have a great impact on the mating system and sexual selection through their effect on population structure. Moreover, the results of this study give further evidence that the opportunity for sexual selection is influenced by the adult sex ratio and hence by the operational sex ratio in a population. Copyright 2002.

A simulation model of the effects of frequency dependence, density dependence and parasitoid flies on the fitness of male field crickets

Post-copulatory sexual selection processes, including sperm competition and cryptic female choice (CFC), can operate based on major histocompatibility (MH) genes. We investigated sperm competition between male alternative reproductive tactics [jack (sneaker) and hooknose (guard)] of Chinook salmon (Oncorhynchus tshawytscha). Using a full factorial design, we examined invitro competitive fertilization success of paired jack and hooknose males at three time points after sperm activation (0, 15 and 60s) to test for male competition, CFC and time effects on male fertilization success. We also examined egg-mediated CFC at two MH genes by examining both the relationship between competitive fertilization success and MH divergence as well as inheritance patterns of MH alleles in resulting offspring. We found that jacks sired more offspring than hooknose males at 0s post-activation; however, jack fertilization success declined over time post-activation, suggesting a trade-off between sperm speed and longevity. Enhanced fertilization success of jacks (presumably via higher sperm quality) may serve to increase sneaker tactic competitiveness relative to dominant hooknose males. We also found evidence of egg-mediated CFC (i.e. female×male interaction) influencing competitive fertilization success; however, CFC was not acting on the MH genes as we found no relationship between fertilization success and MH II β1 or MH I α1 divergence and we found no deviations from Mendelian inheritance of MH alleles in the offspring. Our study provides insight into evolutionary mechanisms influencing variation in male mating success within alternative reproductive tactics, thus underscoring different strategies that males can adopt to attain success.

Female preference for males successful in male–male competition is generally assumed to result in mating with high quality males. Here I report results from an experiment disentangling the effects of intra– and intersexual selection in the sand goby, Pomatoschistus minutus , a marine fish that exhibits paternal care. I show that large males are successful in male–male competition, but contrary to what one would expect, dominants are not preferred by females and are not better at taking care of the eggs. Female preference, however, correlated with the subsequent hatching success of the eggs. Thus, female choice selects for good parenting. Hence, direct benefits in the form of superior paternal care can explain female choice in this species, supporting a good parent process of sexual selection. However, choosing on the outcome of male–male competition does not enable females to mate with the ‘best’ males.

Body size is often a critical determinant of competitive ability and reproductive behavior. For example, small males characteristically lose contests with larger males and may be metabolically constrained from sustaining energetically demanding reproductive behaviors. Small males thus often utilize alternative reproductive tactics (ARTs) to maximize their reproductive success. How variation in body size among behavioral phenotypes arises can provide important insight into the maintenance of ARTs. For instance, smaller body sizes for males adopting ARTs may simply be a function of age, suggesting that the tactic is maintained by the periodic recruitment of young males into the population. Alternatively, body size differences among behavioral phenotypes that are unrelated to age suggest disparate growth rates that potentially arise as a consequence of variation in environmental conditions during development or genotypic differences between the phenotypes. Here we examine these alternative scenarios in the green treefrog, Dryophytes cinereus, using skeletochronological analysis combined with body size measures. As with many other anuran amphibians, male green treefrogs conditionally adopt a noncalling satellite mating tactic and attempt to intercept females attracted to the vocalizations of calling “host” males. We show that males adopting satellite behavior in natural choruses are smaller than calling males but do not represent a class of younger individuals, indicating that satellite males have lower growth rates than calling males. We also show that satellite males are in poorer condition than larger calling males, implicating energetic constraints in size‐related variation in mating tactic expression. Our work suggests that environmental conditions during development, genetic differences between phenotypes, or both, give rise to size discrepancies in behavioral phenotypes, neither of which have been previously explored in anurans. We discuss body size and condition differences between behavioral phenotypes in the context of energetic constraints and endocrine mediation of tactic expression in this species.

Geographic variation in courtship behavior can affect reproductive success of divergent phenotypes via mate choice. Over time, this can lead to reproductive isolation and ultimately to speciation. The Neotropical red‐eyed treefrog (Agalychnis callidryas) exhibits high levels of phenotypic variation among populations in Costa Rica and Panama, including differences in color pattern, body size, and skin peptides. To test the extent of behavioral premating isolation among differentiated populations, we quantified male advertisement calls from six sites and female responses to male stimuli (acoustic and visual signals) from four sites. Our results show that both male advertisement calls and female behavior vary among populations: Discriminant function analyses can predict the population of origin for 99.3% ± 0.7 of males based on male call (dominant frequency and bandwidth) and 76.1% ± 6.6 of females based on female response behavior (frequency and duration of visual displays). Further, female mate choice trials (n = 69) showed that population divergence in male signals is coupled with female preference for local male stimuli. Combined, these results suggest that evolved differences among populations in male call properties and female response signals could have consequences for reproductive isolation. Finally, population variation in male and female behavior was not well explained by geographic or genetic distance, indicating a role for localized selection and/or drift. The interplay between male courtship and female responses may facilitate the evolution of local variants in courtship style, thus accelerating premating isolation via assortative mating.

In Atlantic salmon, as in most salmonids, males can mature early in the life cycle, as small freshwater fish, termed parr, and/or undergo a sea migration before maturing as full–size adults. The alternative life histories are contingent on environmental and social circumstances, such as growth rate, territory quality or any other factor that affects the individual9s state. In order to model the choice of life history in this group of commercially valuable species, it is necessary to understand not only the relative contribution of the different male types to subsequent generations, but also to know the factors that affect reproductive success in each type. In this paper we present the results of a study designed to investigate the factors that affect the reproductive success of mature parr. We used highly polymorphic minisatellite DNA markers to analyse paternity in a series of mating experiments where the number and body size of parr were manipulated. The fraction of eggs fertilized by mature parr ranged from 26 to 40 per cent, with individual parr fertilizing up to 26 per cent of the eggs. A strong positive correlation was found between parr size and reproductive success. The relative success of parr decreased with increasing parr number. Data from this and other studies on variation in the timing and degree of parr reproductive success are discussed in relation to the evolution of male mating strategies and life history in salmonids.

CHAPTER SUMMARY In this chapter we explore the diversity of alternative reproductive tactics (ARTs) exhibited by reptiles. There is a rich literature on ARTs in a broad diversity of reptile lineages, and our contribution is therefore not an exhaustive one. Rather, we attempt to cover topics of general significance to many fields of study, including differences in male and female reproductive behavior, sex ratio adjustment and progeny gender manipulation, and the role of parthenogenesis in mating systems. Our goal is to provide a representative portrait of the diversity of tactics displayed among reptilian lineages, but we often illustrate more elaborate points using data from side-blotched lizards, Uta stansburiana , a system that we have been working on together for a decade. Throughout the chapter we emphasize the distinction between the proximate and the ultimate mechanisms that underlie the evolution of alternative tactics. We conclude with a brief discussion of potentially exciting future research directions in reptilian systems. INTRODUCTION Exploring alternative reproductive tactics (ARTs) in reptiles presents a great challenge given the diverse nature of these taxa. Modern reptilian lineages are paraphyletic with ancient histories. Some extinct reptilian groups such as the dinosaurs undoubtedly exhibited alternative reproductive tactics, given the documented dichotomy between precocial (Geist and Jones 1996, Varricchio et al . 1997) and altricial young (Horner 2000) in various dinosaur lineages. This dichotomy in the developmental tactics of young is strongly associated with the mating systems in the surviving descendants of dinosaurs, the birds.

The social and reproductive behaviour of the dart‐poison frog,Epipedobates femoralis, was studied in Amazonian Peru for 14 months. Males defended territories with advertisement calls and, ultimately, fighting. Territory size ranged from 0.25 to 26 m2and was positively correlated with duration of residence and calling activity of the owner. Females were not territorial and were never attacked when approaching calling males. Males and females only mated once and females sampled calling males before mating. Male mating success was closely correlated with territory size and calling activity. No correlation was found between male body size and mating success. Territories provide residents with sufficient space for mate attraction and reproduction without interference from rivals. Since territory size is dependent on calling activity which involves high energetic costs, it is suggested that territory size reveals male quality.

Alternative reproductive tactics (ARTs) are variable, often discontinuous, behaviours that allow a particular sex to achieve enhanced mating success. Predation risk has been hypothesised to drive the evolution of ARTs, but few empirical studies have examined this. It is unclear whether predators affect fitness of the two sexes directly, by reducing survival, or indirectly, by altering mate searching. In crickets, mate search typically involves acoustic signalling by males and acoustic‐mediated movement towards males by silent females. Males and females may however employ ARTs, which includes silent searching by males, and mating without performing phonotaxis in females. We empirically examined effects of increased predation risk on mate searching behaviour and survival of male and female tree crickets, and their effects on mating success, using field‐enclosure experiments with tree crickets Oecanthus henryi and their primary predator, green lynx spiders Peucetia viridans. Crickets were allocated into three treatments with different levels of predation risk. Increased predation risk strongly reduced survival, and thereby mating success, for both sexes. With increasing predation risk, males reduced calling and increased movement towards neighbouring callers, with negative effects on mating success. By comparing with simulated random movement, we found that male movement was significantly directed towards other calling males, implying a switch to satellite strategies. Female movement behaviour, however, remained unaltered. Males and females thus differed in their response to comparable levels of predation risk, implying that the role of predation as a driver of alternative mate search strategies is sex‐specific. A free Plain Language Summary can be found within the Supporting Information of this article.

The foraging ecology of fish is often considered to be the primary determinant of body shape due to tight links between morphology, swimming performance, and foraging efficiency. Fish foraging on littoral benthic macroinvertebrates typically have a deeper body shape than those foraging on pelagic zooplankton in the water column. However, morphological traits often have multiple ecological functions, which could result in performance trade-offs between functions. Here, we provide the first examination of body shape and diet in a species with alternative reproductive tactics, in this case, bluegill sunfish (Lepomis macrochirus Rafinesque, 1819). Bluegill males mature into either “parental” or “cuckolder” reproductive tactics. Parentals build nests and provide sole parental care and defense of the young. Cuckolders instead act as “sneakers” darting into the nests of parental males while mating is occurring and then later in life become “satellites,” mimicking female appearance and behavior. Using stable carbon and nitrogen isotopic analysis of diet, we found that parentals and females consumed primarily pelagic zooplankton yet were the deepest in body shape. Sneakers consumed more littoral resources but were the most streamlined. Satellite males also consumed predominately littoral resources but had a deeper body form that was more similar to females than to size-matched juveniles. Our results differ from past studies of foraging ecomorphology and suggest that other selection pressures, such as sexual selection in species with alternative reproductive tactics, may also be an important factor influencing shape.