Alternative Mating Strategies Research Articles

A Theoretical Comparison of Alternative Male Mating Strategies in Cephalopods and Fishes.

We used computer simulations of growth, mating and death of cephalopods and fishes to explore the effect of different life-history strategies on the relative prevalence of alternative male mating strategies. Specifically, we investigated the consequences of single or multiple matings per lifetime, mating strategy switching, cannibalism, resource stochasticity, and altruism towards relatives. We found that a combination of single (semelparous) matings, cannibalism and an absence of mating strategy changes in one lifetime led to a more strictly partitioned parameter space, with a reduced region where the two mating strategies co-exist in similar numbers. Explicitly including Hamilton's rule in simulations of the social system of a Cichlid led to an increase of dominant males, at the expense of both sneakers and dwarf males ("super-sneakers"). Our predictions provide general bounds on the viable ratios of alternative male mating strategies with different life-histories, and under possibly rapidly changing ecological situations.

Alternative mating strategies in the Wellington tree weta expressed via genetic polymorphism for precocial male maturation.

The expression of alternative mating strategies is generally hypothesized to be a plastic response of the genome to the environment or a genetic polymorphism. The Wellington tree weta (Hemideina crassidens) is an orthopteran insect in which males express three alternative mating morphotypes related to the size of mandibular weaponry. My common garden experiment in the laboratory shows that male weapon size at maturity in this species is nether condition- nor environment-dependent; therefore, supporting the hypothesis that it is genetically polymorphic. Males that matured at the 8th instar had the shortest development time and the smallest weaponry, males that matured at the 10th instar had the longest development time and the largest weaponry, and males that matured at the 9th instar were intermediate to the other two morphs. These morph-related differences in development time suggest that male alternative mating strategies in this species are expressed via precocial male maturation, a rare mode of strategy expression in insects. Additionally, adult lifespans differed significantly among morphs with 8th instar males having the shortest, and 9th instar males having the longest lifespans. I discuss how these differences in lifespan align with morph-specific investment in pre- and post-copulatory processes to equalize fitnesses among morphs.

Alternative mating strategies in Eurasian Reed Warblers: extra-pair paternity and egg dumping

Alternative mating strategies, involving mating outside a social pair bond, have been studied intensively during the last few decades. However, we are still far from understanding what factors affect their frequencies in wild bird populations. In 2006–2011 we studied Eurasian Reed Warblers breeding in the nature reserve “Stawy Milickie” in SW Poland, and analysed the frequency of extra-pair paternity (EPP) and intra-specific brood parasitism (IBP). We genotyped a total of 786 nestlings from 259 nests. EPP offspring constituted 13.40% of all young (from 7.63% to 22.82% in different study years), and they were found in 21.62% of the broods (from 14.6% to 32.7% annually). The mean proportion of females with EPP young was 24.2% (from 16.2 to 41.7% annually). The proportion of EPP young in nests containing any EPP offspring ranged from 25% to 100% (on average 60%) and was not related to brood size. EPP young in one nest were sired usually by one or two males (92% of all cases), but we recorded one brood with three EPP fathers and one brood of four, where each young was sired by a different EPP male, and none by a social male. We found only one case of intra-specific brood parasitism (IBP). The brood with IBP constituted 0.39% of all examined broods, while the nestling that hatched from the dumped egg constituted 0.13% of all young whose parents were genotyped. We conclude that extra-pair paternity is a relatively common and regularly occurring alternative mating strategy in our study population of Reed Warblers, while intra-specific brood parasitism is extremely rare.

Evaluating the evolutionary mechanisms maintaining alternative mating strategies in a simulated bull trout (Salvelinus confluentus) population.

The coexistence of distinct alternative mating strategies (AMS) is often explained by mechanisms involving trade-offs between reproductive traits and lifetime fitness; yet their relative importance remains poorly understood. Here, we used an established individual-based, spatially explicit model to simulate bull trout (Salvelinus confluentus) in the Skagit River (Washington, USA) and investigated the influence of female mating preference, sneaker-specific mortality, and variation in age-at-maturity on AMS persistence using global sensitivity analyses and boosted regression trees. We assumed that two genetically fixed AMS coexisted within the population: sneaker males (characterized by younger age-at-maturity, greater AMS-specific mortality, and lower reproductive fitness) and territorial males. After 300 years, variation in relative sneaker success in the system was explained by sneaker males' reproductive fitness (72%) and, to a lesser extent, the length of their reproductive lifespan (21%) and their proportion in the initial population (8%). However, under a wide range of parameter values, our simulated scenarios predicted the extinction of territorial males or their persistence in small, declining populations. Although these results do not resolve the coexistence of AMS in salmonids, they reinforce the importance of mechanisms reducing sneaker's lifetime reproductive success in favoring AMS coexistence within salmonid populations but also limit the prediction that, without any other selective mechanisms at play, strong female preference for mating with territorial males and differences in reproductive lifespan allow the stable coexistence of distinct AMS.

Excitatory and inhibitory interactions affect the balance of chorus activity and energy efficiency in the aggregations of male frogs: Numerical simulations using a hybrid dynamical model

We numerically study the role of excitatory and inhibitory interactions in the aggregations of male frogs. In most frogs, males produce sounds to attract conspecific females, which activates the calling behavior of other males and results in collective choruses. While the calling behavior is effective for mate attraction, it requires high energy consumption. In contrast, satellite behavior is an alternative mating strategy in which males deliberately stay silent in the vicinity of a calling male and attempt to intercept the female attracted to the caller, allowing the satellite males to reduce their energy consumption while having a chance of mating. Here we propose a hybrid dynamical model in which male frogs autonomously switch among three behavioral states (i.e., calling state, resting state, and satellite state) due to the excitatory and inhibitory interactions. Numerical simulations of the proposed model demonstrated that (1) both collective choruses and satellite behavior can be reproduced and (2) the satellite males can prolong the energy depletion time of the whole aggregation while they split the maximum chorus activity into two levels over the whole chorusing period. This study highlights the importance of the multiple behavioral types and their transitions for the performance of the whole aggregation.

Greater variability in rhesus macaque (Macaca mulatta) endocranial volume among males than females.

The greater male variability (GMV) hypothesis proposes that traits are more variable among males than females, and is supported by numerous empirical studies. Interestingly, GMV is also observed for human brain size and internal brain structure, a pattern which may have implications for sex-biased neurological and psychiatric conditions. A better understanding of neuroanatomical variability in non-human primates may illuminate whether certain species are appropriate models for these conditions. Here, we tested for sex differences in the variability of endocranial volume (ECV, a proxy for brain size) in a sample of 542 rhesus macaques (Macaca mulatta) from a large pedigreed free-ranging population. We also examined the components of phenotypic variance (additive genetic and residual variance) to tease apart the potential drivers of sex differences in variability. Our results suggest that males exhibit more variable ECVs, and that this pattern reflects either balancing/disruptive selection on male behaviour (associated with alternative male mating strategies) or sex chromosome effects (associated with mosaic patterns of X chromosome gene expression in females), rather than extended neurodevelopment among males. This represents evidence of GMV for brain size in a non-human primate species and highlights the potential of rhesus macaques as a model for sex-biased brain-based disorders.

To self or not to self? Absence of mate choice despite costly outcrossing in the fungus Podospora anserina.

Fungi have a large potential for flexibility in their mode of sexual reproduction, resulting in mating systems ranging from haploid selfing to outcrossing. However, we know little about which mating strategies are used in nature, and why, even in well-studied model organisms. Here, we explored the fitness consequences of alternative mating strategies in the ascomycete fungus Podospora anserina. We measured and compared fitness proxies of nine genotypes in either diploid selfing or outcrossing events, over two generations, and with or without environmental stress. We showed that fitness was consistently lower in outcrossing events, irrespective of the environment. The cost of outcrossing was partly attributed to non-self recognition genes with pleiotropic effects on fertility. We then predicted that when presented with options to either self or outcross, individuals would perform mate choice in favour of the reproductive strategy that yields higher fitness. Contrary to our prediction, individuals did not seem to avoid outcrossing when a choice was offered, in spite of the fitness cost incurred. Our results suggest that, although functionally diploid, P. anserina does not benefit from outcrossing in most cases. We outline different explanations for the apparent lack of mate choice in face of high fitness costs associated with outcrossing, including a new perspective on the pleiotropic effect of non-self recognition genes.

Sex-specific morphs: the genetics and evolution of intra-sexual variation.

Sex-specific morphs exhibit discrete phenotypes, often including many disparate traits, that are observed in only one sex. These morphs have evolved independently in many different animals and are often associated with alternative mating strategies. The remarkable diversity of sex-specific morphs offers unique opportunities to understand the genetic basis of complex phenotypes, as the distinct nature of many morphs makes it easier to both categorize and compare genomes than for continuous traits. Sex-specific morphs also expand the study of sexual dimorphism beyond traditional bimodal comparisons of male and female averages, as they allow for a more expansive range of sexualization. Although ecological and endocrinological studies of sex-specific morphs have been advancing for some time, genomic and transcriptomic studies of morphs are far more recent. These studies reveal not only many different paths to the evolution of sex-specific morphs but also many commonalities, such as the role of sex-determining genes and hormone signalling in morph development, and the mixing of male and female traits within some morphs.

Evolutionary Ecology of Fixed Alternative Male Mating Strategies in the Ruff (Calidris pugnax)

A few empirical examples document fixed alternative male mating strategies in animals. Here we focus on the polymorphism of male mating strategies in the ruff (Calidris pugnax, Aves Charadriiformes). In ruffs, three fixed alternative male mating strategies coexist and are signaled by extreme plumage polymorphism. We first present relevant data on the biology of the species. Then we review the available knowledge of the behavioral ecology of ruffs during the breeding season, and we detail the characteristics of each of the three known fixed male mating strategies. We next turn to the results of exceptional quality accumulated on both the structural and functional genomics of the ruff over the past few years. We show how much these genomic data can shed new, mechanistic light on the evolution and maintenance of the three fixed alternative male mating strategies. We then look if there is sufficient indication to support frequency-dependent selection as a key mechanism in maintaining these three strategies. Specifically, we search for evidence of equal fitness among individuals using each of the three strategies. Finally, we propose three lines of research avenues that will help to understand the eco-evolutionary dynamics of phenotypic differences within natural populations of this iconic model species.

A re‐assessment of within‐host mating behavior in the Nasonia species complex

AbstractInsects have a wide variety of mating systems. For parasitic wasps, mating sites are often confined to where their hosts occur and this mutual interaction therefore greatly affects the evolution of alternative mating strategies. Parasitoids of the genus Nasonia (Hymenoptera: Pteromalidae) – comprising the species Nasonia vitripennis (Walker), Nasonia longicornis Darling, Nasonia giraulti Darling, and Nasonia oneida Raychouhury & Desjardins – parasitize blowfly pupae and typically mate immediately after emergence of the females from the host puparium. However, in one Nasonia species, N. giraulti, mating predominantly occurs within the host. Here, we re‐assess within‐host mating (WHM) rates within the Nasonia genus, using laboratory lines and field‐collected hosts, including N. oneida for which no data were available yet. We confirm that WHM rates are low in N. vitripennis and N. longicornis, but high in N. giraulti. WHM is rare in N. oneida, despite its sympatry and close phylogenetic relationship with N. giraulti. Multiparasitization experiments with N. vitripennis and N. giraulti resulted in lower WHM proportions of N. giraulti. To evaluate whether this was due to an exit hole in the host pupa created by N. vitripennis males – where an exit hole may result in emergence of N. giraulti females and possibly males prior to mating – we artificially created exit holes in the host parasitized by N. giraulti only. This also yielded a lower WHM proportion. Progeny analysis of interspecific crosses of N. longicornis and N. oneida with N. giraulti, generating hybrid female but non‐hybrid male offspring, revealed that WHM is largely determined by the maternal species and, hence, by the species to which the male offspring belong. We conclude that WHM is predominantly a male‐mediated trait in N. giraulti, resulting from males refraining from making exit holes and mating with females inside the host. We discuss how these findings can be used to evaluate whether WHM contributes to preventing species hybridization.

Environmental drivers of sexual dimorphism in a lizard with alternative mating strategies.

Understanding the relative importance of sexual and natural selection in shaping morphological traits is a long-standing goal of evolutionary ecology. Male-biased sexual size dimorphism (SSD) is typically associated with male-male competition. Similarly, male polymorphisms are considered a consequence of competitive social interactions. This classic paradigm overlooks the fact that environmental factors mediate social interactions and can lead to ecological adaptations. Common side-blotched lizards, Uta stansburiana, are a model system for this paradigm due to well-known rock-paper-scissors social dynamics between male morphs. SSD in this species has been considered primarily a consequence of social interactions, with male size resulting from the number of morphs in each population and female size being constrained through fecundity benefits. We test if the environment explains intraspecific variation in SSD and number of male morphs in U.stansburiana. By compiling data from 49 populations, we show that environmental variables are stronger predictors of SSD than the number of male morphs. Similarly, we show that the environment mediates SSD and potentially contributes to morph loss in colder environments. We propose that the environment favours smaller males in areas of high seasonality. Our results demonstrate the importance of the environment as a mediator of SSD.

Reproductive Strategies Change With Time in a Newly Founded Colony of Spotless Starlings (Sturnus unicolor)

Variation in avian reproductive strategies is often studied from a comparative perspective, since even closely-related taxa differ greatly in the degree of polygyny, extra-pair paternity (EPP) or intra-specific brood-parasitism. However, substantial variation at the species level suggests that ecological factors are important in shaping these patterns. In this study, we examined the temporal plasticity of these strategies, following a population from the year of colony formation to 2 years after this. Parentage data from these years shows that polygyny decreased with time, likely as a consequence of increased competition for nesting sites and mates by new recruits, and immigrants of higher quality arriving to the colony as time passed. In parallel to this temporal change, we found an increase in intra-specific brood-parasitism and quasi-parasitism (QP). We interpret these patterns as a consequence of an increase of floaters with time; these birds pursue a mixture of alternative mating strategies to succeed in the population. We also found evidence of conspecific brood parasitism (CBP), by nesting females that laid part of the clutch in another nest or that after losing a partially laid clutch resorted to lay the last eggs in another nest. Analyses of the distance between the main nest and nests containing the secondary polygynous brood or extra-pair or parasitic young showed an avoidance of contiguous nests for conducting these alternative reproductive tactics. At the same time, these secondary nests were closer to the main nest than random distances within the colony, suggesting that access to public information was restricted to a narrow area around the main nest. Our study emphasizes how behavioral patterns are plastic traits that vary not only with individual circumstances, but also with time, tracking changes in density and social structure.

Double-digest RAD sequencing reveals low rates of conspecific brood parasitism and no cases of quasi-parasitism in a Neotropical passerine

Levels of conspecific brood parasitism (CBP) and quasi-parasitism (QP) are important parameters for the general understanding of alternative female mating strategies. We deployed double-digest RAD sequencing to assess CBP and QP in a south temperate population of Grass Wrens (Cistothorus platensis). CBP rate was low and varied annually (0–10%). No cases of QP were identified in our population. Grass Wrens showed similar levels of CBP when compared to other Neotropical songbirds. Given that females could increase their reproductive output by laying eggs in both their nests and in other females' nests, it is striking that CBP is so rare. Future work should evaluate counter-adaptations (egg pecking and rejection, nest desertion, and retaliation) that reduce the success of CBP.

Multi-year pair-bonding in Murray cod (Maccullochella peelii)

Mating strategies in fishes are known to include polygyny, polyandry and monogamy and provide valuable insights regarding powerful evolutionary forces such as sexual selection. Monogamy is a complex of mating systems that has been relatively neglected. Previous work on mating strategies in fishes has often been based on observation and focused on marine species rather than freshwater fishes. SNPs are increasingly being used as a molecular ecology tool in non-model organisms, and methods of probabilistic genetic analysis of such datasets are becoming available for use in the absence of parental genotypes. This approach can be used to infer mating strategies. The long-term pair bonding seen in mammals, reptiles and birds has not been recorded in freshwater fishes—in every other respect an extremely diverse group. This study shows that multi-year pair bonding occurs in an Australian Percichthyid fish that exhibits paternal care of eggs and larvae. Using SNPs, full sibling pairs of larvae were found over multiple years in a three-year study. Stable isotope signatures of the larvae support the genetic inference that full sibling pairs shared a common mother, the ultimate source of that isotopic signature during oogenesis. Spatial and temporal clustering also suggests that the full sibling larvae are unlikely to be false positive identifications of the probabilistic identification of siblings. For the first time, we show multi-year pair bonding in a wild freshwater fish. This will have important conservation and management implications for the species. This approach could provide insights into many behavioural, ecological and evolutionary questions, particularly if this is not a unique case. Our findings are likely to initiate interest in seeking more examples of monogamy and alternative mating strategies in freshwater fishes, particularly if others improve methods of analysis of SNP data for identification of siblings in the absence of parental genotypes.

Cryptic alternative male mating strategies in invasive alien round goby (Neogobius melanostomus) of the upper Danube River

Male alternative mating strategies are a widespread life history choice, yet they have hardly been assessed in the context of fish invasions. As established proxies for alternative life-history strategies, body length and sexual maturity of Ponto–Caspian round goby (Neogobius melanostomus) from the recently invaded upper Danube River were contrasted and differential trophic niche occupation was assessed. Only about 4% of analyzed gobies qualified as potential sneakers which may be explained by the recent and ongoing invasion process. This study provides evidence for the occurrence of sneaking behavior of invasive round goby in the upper Danube River.

Equal fitness among alternative mating strategies in a harem polygynous insect.

Alternative mating strategies are widespread among animal taxa, with strategies controlled by a genetic polymorphism (Mendelian strategy) being rarer in nature than condition-dependent developmental strategies. Mendelian strategies are predicted to have equal average fitnesses and the proportion of offspring produced by a strategy should equal the equilibrium proportion of individuals representing the strategy in a population. Developmental strategies are not expected to produce offspring in equilibrium proportions; however, whether the alternative phenotypes should have equal average fitness is debated. The Wellington tree wētā (Hemideina crassidens) (Orthoptera: Anostostomatidae) is a harem polygynous insect in which intense sexual competition has favoured the evolution of three alternative mating strategies that differ in weapon size and the ability to fight for control of harems. Here, we use molecular genotyping to test the hypothesis that the alternative strategies in this species are maintained by having equal relative fitness and that morphs produce offspring in equilibrium proportions. As expected, the average relative fitness of the three strategies did not significantly differ and the proportion of offspring produced by each morph is equal to the frequency of that morph in the population. Our results support the hypothesis that the alternative male morphs in H. crassidens represent Mendelian strategies.

Identification of Follower Status Based on Male Proximity Score in Crested Macaque

Crested macaque live in multimale-multifemale social groups where temporary association (consortship) typically occurs. Current theory and these limited qualitative observations suggest the hypothesis that behavior functions as a means for males to gain access to fertile females. The aim of this study was to investigate follower status based on quantitative method. Males were classified as either “consort males,” “followers,” and “non-followers” based on proximity maintanance every 15 minute uses scan sampling. Tactics used by followers were classified into 1) individual challenge, 2) coalitionary challenge, 3) abandoned takeover, and 4) opportunistic takeover. The proportion of successful takeovers by followers was calculated by dividing the number of takeovers by followers by the total number of observed takeovers. The proportion of followers is higher than average on D-5 and earlier, D-4, and D-3. Only two of the four consort takeover tactics were used by followers. For abandoned which made up 40% and for individual tactic was made up to 11.5% of consort takeovers tactic used. This study contribute to our understanding of alternative mating strategy in primate and provide the first quantitative data demonstrating that following is an alternative mating strategy in crested macaque (Macaca nigra).

Relative sexual attractiveness does not influence mate-choice copying in male Trinidadian guppies, Poecilia reticulata

Copying the mate choice of another conspecific by a bystanding observer is a socially mediated alternative mating strategy to independent mate choice. Because increased sperm competition is a potential cost of mate-choice copying, males should be prudent and less likely to copy the observed mate choice of other males when the latter are more sexually attractive than themselves. We tested this hypothesis using the Trinidadian guppy, Poecilia reticulata. Focal observer males were simultaneously presented with a large and a small female as potential mates, either in the presence or absence of a nearby model male. We varied the relative differences in the body length and colour ornamentation, traits that predict male sexual attractiveness and competitiveness in the guppy, of observer and model males in each of three experimental treatments: (1) observer and model males were matched for body length and colour ornamentation; (2) the model male was larger and more colourful than the observer male; (3) the model male was smaller and less colourful than the observer male. We compared the mating preferences of focal observer males in each of the latter treatments with that of focal males in a control treatment, wherein no model male (and thus no copying opportunity) was present. As predicted, focal males copied the staged apparent mate choice of a model male in all three experimental treatments, but not in the control treatment. However, contrary to our a priori hypothesis, there were no significant differences in the likelihood or strength of the copying response in observer males among the experimental treatments. Although male guppies are known to modify their mating tactics in the presence of sexual competitors, we found no evidence for an influence of the relative phenotypes of observer and model males on mate-choice copying behaviour in focal observer males.

Spatial position-associated mating strategies employed by male Japanese macaques (Macaca fuscata yakui) in Yakushima.

In bisexual groups, dominant males occupy the central part of the group, which is advantageous because it is reproductively beneficial. However, high-ranking males do not necessarily monopolize reproductive success, which indicates that low-ranking males increase their reproductive success through alternative mating strategies. To reveal the effectiveness and cost of these strategies employed by group males, it is necessary to clarify the spatial configuration of males and their group, and show how males combine strategies in different situations. This study demonstrates the spatial configuration of male Japanese macaques (Macaca fuscata yakui) and their group when males adopt three mating strategies: mate guarding, sneak mating, and cross-boundary mating (mating with females of another group). High-ranking males tended to perform mate guarding, but they also mated with females in other groups when there were few sexually active females in their group. Low-ranking males performed sneak mating; they remained in the central part of the group to monitor sexually active females and moved toward the periphery for copulation but never completely left the group. In addition, males individually ventured outside the group's ranging area and succeeded in mating with females of other groups. The cross-boundary mating strategy has the advantage of increasing the number of potential mating partners, which is not present in the other two strategies. However, because of considerable costs and low contribution to mating frequency, this strategy is complementary and is employed when the expectation of mating success in their group is low.

Environmental influences on life history strategies in partially anadromous brown trout (Salmo trutta, Salmonidae)

AbstractThis paper reviews the life history of brown trout and factors influencing decisions to migrate. Decisions that maximize fitness appear dependent on size at age. In partly anadromous populations, individuals that attain maturity at the parr stage typically become freshwater resident. For individual fish, the life history is not genetically fixed and can be modified by the previous growth history and energetic state in early life. This phenotypic plasticity may be influenced by epigenetic modifications of the genome. Thus, factors influencing survival and growth determine life‐history decisions. These are intra‐ and interspecific competition, feeding and shelter opportunities in freshwater and salt water, temperature in alternative habitats and flow conditions in running water. Male trout exhibit alternative mating strategies and can spawn as a subordinate sneaker or a dominant competitor. Females do not exhibit alternative mating behaviour. The relationship between growth, size and reproductive success differs between sexes in that females exhibit a higher tendency to migrate than males. Southern populations are sensitive to global warming. In addition, fisheries, aquaculture with increased spreading of salmon lice,introduction of new species, weirs and river regulation, poor water quality and coastal developments all threaten trout populations. The paper summarizes life‐history data from six populations across Europe and ends by presenting new research questions and directions for future research.