Alternative Reproductive Tactics Research Articles

Spatial structure could explain the maintenance of alternative reproductive tactics in tree cricket males.

Trait polymorphisms are widespread in nature, and explaining their stable co-existence is a central problem in ecology and evolution. Alternative reproductive tactics, in which individuals of one or more sex exhibit discrete, discontinuous traits in response to reproductive competition, represent a special case of trait polymorphism in which the traits are often complex, behavioural, and dynamic. Thus, studying how alternative reproductive tactics are maintained may provide general insights into how complex trait polymorphisms are maintained in populations. We construct a spatially explicit individual-based model inspired from extensively collected empirical data to address the mechanisms behind the co-existence of three behavioural alternative reproductive tactics in males of a tree cricket (Oecanthus henryi). Our results show that the co-existence of these tactics over ecological time scales is facilitated by the spatial structure of the landscape they inhabit, which serves to equalize the otherwise unequal mating benefits of the three tactics. We also show that this co-existence is unlikely if spatial aspects of the system are not considered. Our findings highlight the importance of spatial dynamics in understanding ecological and evolutionary processes and underscore the power of integrative approaches that combine models inspired from empirical data.

Ecological correlates of alternative reproductive tactics: conspecific brood parasitism rates vary with nest predation and seasonal effects influenced by climate change

Ecological and social factors shape individual reproductive strategies. Climate change has wide‐ranging effects on the timing of reproduction and availability of nesting sites for many birds. Ecological factors such as season length or predation rate could in turn affect the relative success rates of alternative reproductive tactics (ARTs). A new article by Pöysä (2024) featuring a long‐term study of common goldeneyes Bucephala clangula highlights the role of climate change in altering rates of conspecific brood parasitism (CBP) by affecting nest initiation dates and season length. While some authors have emphasized the effects of spatial and temporal aggregation of nests in promoting tactics of reproductive interference, few studies have addressed the effects of environmental variables on rates of CBP and other ARTs. I review some of the evidence for a relationship between population‐level nest predation rate and rates of CBP, principally in ducks and rails, and suggest a role for high rates of nest loss from all sources in the evolution of CBP and host responses. There is a need for further studies that examine environmental correlates of ARTs. Long‐term studies have the highest potential to reveal how shifts in phenology and life history variables may respond to environmental perturbations. Comparative studies of similar species in remote geographic locations can add perspective of how different ecological variables affect the prevalence of ARTs.

Squid male alternative reproductive tactics are determined by birth date.

Alternative reproductive tactics (ARTs) are discontinuous phenotypes associated with reproduction, observed in males of many species. Typically, large males adopt a tactic of competing with rivals for mating, while small males adopt a tactic of stealing fertilization opportunities from the large males. The 'birth date hypothesis', proposing that the date of birth influences the determination of each male's reproductive tactic, has been tested only in teleost fish to date. Here, the birth date hypothesis was tested in ARTs of Japanese spear squid Heterololigo bleekeri (consort/sneaker) by analysing statolith growth increments. The birth date significantly differed between consorts (early-hatched) and sneakers (late-hatched). However, no differences were detected in growth history up to 100 days from hatching. Most immature males caught during the reproductive season were larger than sneakers, and their hatch date was similar to that of consorts, suggesting that these immature males had already been following a life-history pathway as a consort. These results indicate that ARTs of H. bleekeri are determined based on their hatch date in early life. This study firstly suggests that the birth date hypothesis applies to aquatic invertebrates, suggesting that the mechanism by which birth date determines the individual phenotype is a phenomenon more common than previously believed.

Nest predation and climate change as drivers of alternative reproductive tactics in a migratory species

Alternative reproductive tactics enable individuals to choose a reproductive tactic relative to their status and prevailing environmental conditions in a way that increases their fitness. For example, females in many avian species show phenotypic plasticity and employ alternative reproductive tactics to cope with changes in predation risk and climate. Conspecific brood parasitism (CBP), in which females lay eggs in nests of conspecifics, is one example of such behaviour. It has been proposed that when prospects for successful nesting are low and/or costs of reproduction are high, females employ tactics of low effort such as non‐breeding and parasitic laying. When environmental conditions are ideal and prospects for success high, females can increase their reproductive effort above typical nesting by laying parasitic eggs prior to initiating their own nest. Here, I used this flexible life‐history strategy concept and long‐term (1994‒2022) population level data of the common goldeneye Bucephala clangula to study how the rate of parasitic laying varies in relation to variation in nest predation risk and in the timing and length of the breeding season, the latter being measured by the timing of ice breakup. Nest predation rate in the previous year and timing of ice breakup interactively affected parasitic laying, the rate of parasitic laying being particularly high in years with late ice breakup and high nest predation rate in the previous year. Furthermore, the proportion of predated eggs was lower in parasitized nests than in non‐parasitized nests, while the opposite was true for the proportion of eggs that failed in other way. As a consequence, the final number of young produced per nest was higher for parasitized nests. The findings of this study show that changes in environmental conditions affect the dynamics of alternative reproductive tactics in goldeneyes, with consequences to population level reproductive output.

Genetically identical mice express alternative reproductive tactics depending on social conditions in the field.

In many species, establishing and maintaining a territory is critical to survival and reproduction, and an animal's ability to do so is strongly influenced by the presence and density of competitors. Here we manipulate social conditions to study the alternative reproductive tactics displayed by genetically identical, age-matched laboratory mice competing for territories under ecologically realistic social environmental conditions. We introduced adult males and females of the laboratory mouse strain C57BL/6J into a large, outdoor field enclosure containing defendable resource zones under one of two social conditions. We first created a low-density social environment, such that the number of available territories exceeded the number of males. After males established stable territories, we introduced a pulse of intruder males and observed the resulting defensive and invasive tactics employed. In response to this change in social environment, males with large territories invested more in patrolling but were less effective at excluding intruder males as compared with males with small territories. Intruding males failed to establish territories and displayed an alternative tactic featuring greater exploration as compared with genetically identical territorial males. Alternative tactics did not lead to equal reproductive success-males that acquired territories experienced greater survival and had greater access to females.

Alternative reproductive tactics and evolutionary rescue

Abstract 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.

Flanged males have higher reproductive success in a completely wild orangutan population.

Male orangutans (Pongo spp.) exhibit bimaturism, an alternative reproductive tactic, with flanged and unflanged males displaying two distinct morphological and behavioral phenotypes. Flanged males are larger than unflanged males and display secondary sexual characteristics which unflanged males lack. The evolutionary explanation for alternative reproductive tactics in orangutans remains unclear because orangutan paternity studies to date have been from sites with ex-captive orangutans, provisioning via feeding stations and veterinary care, or that lack data on the identity of mothers. Here we demonstrate, using the first long-term paternity data from a site free of these limitations, that alternative reproductive tactics in orangutans are condition-dependent, not frequency-dependent. We found higher reproductive success by flanged males than by unflanged males, a pattern consistent with other Bornean orangutan (Pongo pygmaeus) paternity studies. Previous paternity studies disagree on the degree of male reproductive skew, but we found low reproductive skew among flanged males. We compare our findings and previous paternity studies from both Bornean and Sumatran orangutans (Pongo abelii) to understand why these differences exist, examining the possible roles of species differences, ecology, and human intervention. Additionally, we use long-term behavioral data to demonstrate that while flanged males can displace unflanged males in association with females, flanged males are unable to keep other males from associating with a female, and thus they are unable to completely mate guard females. Our results demonstrate that alternative reproductive tactics in Bornean orangutans are condition-dependent, supporting the understanding that the flanged male morph is indicative of good condition. Despite intense male-male competition and direct sexual coercion by males, female mate choice is effective in determining reproductive outcomes in this population of wild orangutans.

Modelling the impacts of male alternative reproductive tactics on population dynamics.

Observations of male alternative reproductive tactics (ARTs) in a variety of species have stimulated the development of mathematical models that can account for the evolution and stable coexistence of multiple male phenotypes. However, little attention has been given to the population dynamic consequences of ARTs. We present a population model that takes account of the existence of two male ARTs (guarders and sneakers), assuming that tactic frequencies are environmentally determined and tactic reproductive success depends on the densities of both types. The presence of sneakers typically increases overall population density. However, if sneakers comprise a sufficiently large proportion of the population-or, equivalently, if guarders are sufficiently rare-then it is possible for the total population to crash to extinction (in this extreme regime, there is also an Allee effect, i.e. a threshold density below which the population will go extinct). We apply the model to the example of the invasive round goby (Neogobius melanostomus). We argue that ARTs can dramatically influence population dynamics and suggest that considering such phenotypic plasticity in population models is potentially important, especially for species of conservation or commercial importance.

Female reproductive fluid and male seminal fluid: a non-gametic conflict for post-mating control.

Growing evidence shows that non-gametic components released by both males and females can significantly drive sperm competition outcomes. Seminal fluid (SF) was shown to influence paternity success by affecting rival males' sperm performance, and, in some species with male alternative reproductive tactics, to selectively decrease the fertilization success of males of the opposite tactic. Female reproductive fluid (FRF) has been proven to differentially influence ejaculates of different males and bias fertilization towards specific partners. Whether, and with what outcome, these two processes can intersect to influence sperm competition is still unknown. Here we explore this scenario in the grass goby (Zosterisessor ophiocephalus), a fish with territorial-sneaker reproductive tactics, where sneaker males can exploit the territorials' SF while penalizing territorial sperm performance with their own fluid. To test whether FRF can rebalance the ejaculate competition in favour of territorial males, we used in vitro fertilization with a SF mixture (territorial + sneaker), using increasing concentrations of FRF, to simulate the natural conditions that ejaculates encounter towards the eggs. Our findings revealed a differential effect of FRF on the different tactics' fertilization success, favouring territorial ejaculates, possibly through an attenuation of the detrimental effects of sneaker SF, and enabling females to regain control over the fertilization process.

Alternative reproductive tactics in goby fishes of the Caspian Sea.

Here we report on the reproductive morphology and histology of three Gobiidae species (the Caspian monkey goby, Neogobius pallasi; the Caspian goby, Neogobius caspius; and the round goby, Neogobius melanostomus) from the Iranian coastline of the Caspian Sea. Based on ageing, reproductive histology, and internal and external morphological measures, it appears that all three of these goby species have two types of reproductive males, a large courting, territorial, male type and a small cuckolding parasitic male type, a phenomenon known as alternative reproductive tactics (ART). Although ARTs have been reported previously for one of these species, the round goby, all reports stem from its invasive range; ARTs have never been reported before in any fish species in the Caspian Sea. In all three goby species there was a large, older male type, with a wide head, dark body colouration, and a large investment in accessory glands (AG), an organ important for female attraction and parental care. But there was also a small, light, younger male type, with a narrow head, longer urogenital papilla, and little investment in AGs. The Caspian goby were the largest of the three species, and in this species the smaller, lighter, presumably cuckolding male morph was quite rare (only about 5% of the reproductive male population). In contrast, many of the round goby and monkey goby males were the small, lighter parasitic type, making up nearly half the population of reproductive males (48% and 40%, respectively). Round goby and Caspian goby males had a prominent mesorchial gland, a fibrous sheath of pheromone-releasing connective tissue that attaches the testes to the dorsal body wall, but all the monkey goby specimens examined lacked this structure. Although ARTs are well documented across fish species and appear to be particularly common in gobies, our study provides the first evidence for ARTs in goby fishes from the Caspian Sea.

The operational sex ratio experienced by mothers modulates the expression of sons’ alternative reproductive tactics in spider mites

The operational sex ratio experienced by mothers modulates the expression of sons’ alternative reproductive tactics in spider mites

Alternative reproductive tactics of unflanged and flanged male orangutans revisited.

In many slowly developing mammal species, males reach sexual maturity well before they develop secondary sexual characteristics. Sexually mature male orangutans have exceptionally long periods of developmental arrest. The two male morphs have been associated with behavioral alternative reproductive tactics, but this interpretation is based on cross-sectional analyses predominantly of Northwest Sumatran populations. Here we present the first longitudinal analyses of behavioral changes of 10 adult males that have been observed in both unflanged and flanged morph. We also analyzed long-term behavioral data on an additional 143 individually identified males from two study sites, Suaq (Sumatra, Pongo abelii) and Tuanan (Borneo, Pongo pygmaeus wurmbii), to assess male mating tactics cross-sectionally in relation to population, male morph (unflanged and flanged), and other socio-ecological factors. Both our longitudinal and cross-sectional results confirm and refine previous cross-sectional accounts of the differences in mating tactics between the unflanged and the flanged male morphs. In the unflanged morph, males exhibit higher sociability, particularly with females, and higher rates of both copulation and sexual coercion than in the flanged morph. Based on our results and those of previous studies showing that females prefer flanged males, and that flanged males have higher reproductive success, we conclude that unflanged males face a trade-off between avoiding male-male contest competition and gaining mating access to females, and thus follow a "best-of-a-bad-job" mating strategy.

Genotype and growth rate influence female mate preference in Xiphophorus multilineatus: Potential selection to optimize mortality-growth rate tradeoff.

The extent to which mate preferences are adaptive requires a better understanding of the factors that influence variation in mate preferences. Xiphophorus multilineatus is a live-bearing fish with males that exhibit alternative reproductive tactics (courter/sneaker). We examined the influence of a female's genotype (courter vs sneaker lineage), growth rate, and social experience on mate preference for courter as compared to sneaker males. We found that females with a sneaker genotype and slower growth rates had stronger mate preferences for the faster growing courter males than females with a courter genotype, regardless of mating experience with one or both types of males. In addition, the relationship between strength of preference and growth rate depended on a females' genotype; females with sneaker genotypes decreased their preference as their growth rates increased, a pattern that trended in the opposite direction for females from the courter genotypes. Disassortative mating preferences are predicted to evolve when heterozygous offspring benefit from increased fitness. Given male tactical dimorphism in growth rates and a mortality-growth rate tradeoff previously detected in this species, the variation in mating preferences for the male tactics we detected may be under selection to optimize the mortality-growth rate tradeoff for offspring.

Social Environment Influences the Temporal Dynamics of Sneak-Spawning in a Fish with Alternative Reproductive Tactics.

AbstractSeveral predictions of sperm competition theory are not well supported empirically. One potential reason is that most current theory and empirical research ignore how the social environment influence the temporal dynamics of mating. We propose that understanding these dynamics is key to understanding sexual selection and improving the predictive power of theory. To demonstrate the importance of these dynamics, we quantify how males' social role, interactions among males, and current social environment influence the timing of mating in Symphodus ocellatus, a species with three alternative male reproductive tactics. Nesting males spawn synchronously with females; sneakers and satellites sneak-spawn with some time delay. Satellites also cooperate with nesting males. We found that satellites have shorter sneak-spawning delays than sneakers, a benefit of their cooperation with nesting males. Sneak-spawning delays decreased with increasing nest activity for sneakers but not for satellites, suggesting that sneakers may benefit from increased sperm competition intensity. Current sperm competition models ignore this potential benefit, which may be why the prediction that males should decrease investment when sperm competition involves more than two males is not well supported. Our study provides insight into mechanisms that drive variation in the timing of spawning, which could explain mismatches between theoretical and empirical results.

Physiological costs to behavioural plasticity in a swordtail fish: clues to its evolutionary maintenance and loss

Behavioural plasticity may require energetically expensive sensory and neural adaptations to detect, process and respond to social cues. These costs could lead to selection against behavioural plasticity and its eventual loss. We found that males from the behaviourally plastic alternative reproductive tactic (ART) in the swordtail fish Xiphophorus multilineatus had relatively larger brains, in addition to a trade-off with testes size, that was not detected in the males from the behaviourally fixed ART. Given these costs, we consider the hypothesis that plasticity in mating behaviours is maintained due to intralocus tactical conflict, where a shared genome can constrain one or both ARTs from evolving to their optima. When we reduced any potential for intralocus tactical conflict by removing the behaviourally fixed ART from long-term breeding mesocosms, males from the behaviourally plastic ART were less plastic and had smaller brains compared to their counterparts from control mesocosms (both male ARTs). We also detected evidence for a genetic correlation between the ARTs for behaviour, which is required for intralocus conflict. Our findings suggest that intralocus tactical conflict could be maintaining behavioural plasticity, in which case behavioural plasticity may not be adaptative in some cases.

Age-specific survival of territorial and non-territorial male chamois.

How alternative reproductive tactics (ARTs) are maintained in wildlife populations is one of the major questions in evolutionary biology. As a dominant status, territoriality is typically linked to increased mating opportunities, and one explanation why this behaviour coexists with other tactics is that dominance implies survival costs. Such a trade-off may occur in the Northern chamois Rupicapra rupicapra, as reproductive advantages of territorial males over non-territorial males could be counterbalanced by a reduction in survival mediated through energy expenditure, stress and parasitic infections, ultimately favouring ART coexistence. Here, we analysed age-dependent survival probabilities of territorial (n = 15) and non-territorial (n = 16) adult chamois using information collected over 12 years between 2010 and 2021 in the Gran Paradiso National Park (Western Italian Alps). Survival rates were estimated with a CMR approach using Burnham's joint modelling of live encounter and dead recovery data. The model selection procedure, based on AICc value minimisation, supported a linear decrease of survival with age but the results did not match our predictions, as territorial chamois did not have lower survival rates than non-territorial chamois. In contrast, territorial males appeared to enjoy reproductive success at lower survival costs. This, in turn, supports the role of other factors, such as snow-dependent environmental stochasticity, in the maintenance of ARTs in chamois populations. The limited sample size, however, calls for caution in interpretation, and long-term studies of lifetime reproductive success and survival are necessary to clarify the mechanisms underlying the expression and coexistence of different reproductive behaviours in this species.

Mountain ungulate mating systems: patterns and processes

ABSTRACTMountain ungulates of the subfamily Caprinae, including wild sheep, goats and goat‐antelopes, show remarkable interspecific diversity in habitat preferences, social organisation and morphological features. We review how this diversity relates to their mating behaviour.After introducing the ecology of mating systems and the evolution of the Caprinae, we investigate the pairwise, sequential relationships between habitat preferences, social behaviour, level of polygyny, and morphological features, and discuss the ecological processes underlying the patterns of mate monopolisation and acquisition.From forest‐dwelling, solitary, monogamous and monomorphic goat‐antelopes, to highly dimorphic, polygynous and social wild sheep and goats inhabiting open landscapes, mountain ungulates reveal a close relationship between habitat openness and sexual dimorphism, through the level of sociality and that of mate monopolisation.Although over the last few decades some information has been collected on the biology of Caprinae, our understanding of determinants of their mating systems is still hampered by limited data to estimate opportunities for sexual selection, as well as uncertainties over the occurrence and maintenance of alternative reproductive tactics, and lack of information on female mate choice.The study of mating systems and that of the factors influencing them play a key role from an evolutionary and conservation standpoint. This is relevant to the Caprinae, whose main habitat is expected to be strongly affected by the ongoing climatic change, with potential effects on the phenology of their mating systems, and whose economic value is relevant for consumptive and nonconsumptive uses. A better understanding of the diversity and ecology of mating systems will require a wealth of additional field observations on male and female behaviour, as well as genetic assessments of reproductive success.

Individual reflectance of solar radiation confers a thermoregulatory benefit to dimorphic males bees (Centris pallida) using distinct microclimates.

Incoming solar radiation (wavelengths 290-2500 nm) significantly affects an organism's thermal balance via radiative heat gain. Species adapted to different environments can differ in solar reflectance profiles. We hypothesized that conspecific individuals using thermally distinct microhabitats to engage in fitness-relevant behaviors would show intraspecific differences in reflectance: we predicted individuals that use hot microclimates (where radiative heat gain represents a greater thermoregulatory challenge) would be more reflective across the entire solar spectrum than those using cooler microclimates. Differences in near-infrared (NIR) reflectance (700-2500 nm) are strongly indicative of thermoregulatory adaptation as, unlike differences in visible reflectance (400-700 nm), they are not perceived by ecological or social partners. We tested these predictions in male Centris pallida (Hymenoptera: Apidae) bees from the Sonoran Desert. Male C. pallida use alternative reproductive tactics that are associated with distinct microclimates: Large-morph males, with paler visible coloration, behave in an extremely hot microclimate close to the ground, while small-morph males, with a dark brown dorsal coloration, frequently use cooler microclimates above the ground near vegetation. We found that large-morph males had higher reflectance of solar radiation (UV through NIR) resulting in lower solar absorption coefficients. This thermoregulatory adaptation was specific to the dorsal surface, and produced by differences in hair, not cuticle, characteristics. Our results showed that intraspecific variation in behavior, particular in relation to microclimate use, can generate unique thermal adaptations that changes the reflectance of shortwave radiation among individuals within the same population.

Genomic basis of Y-linked dwarfism in cichlids pursuing alternative reproductive tactics.

Sexually antagonistic selection, which favours different optima in males and females, is predicted to play an important role in the evolution of sex chromosomes. Body size is a sexually antagonistic trait in the shell-brooding cichlid fish Lamprologous callipterus, as "bourgeois" males must be large enough to carry empty snail shells to build nests whereas females must be small enough to fit into shells for breeding. In this species, there is also a second male morph: smaller "dwarf" males employ an alternative reproductive strategy by wriggling past spawning females into shells to fertilize eggs. L.callipterus male morphology is passed strictly from father to son, suggesting Y-linkage. However, sex chromosomes had not been previously identified in this species, and the genomic basis of size dimorphism was unknown. Here we used whole-genome sequencing to identify a 2.4-Mb sex-linked region on scaffold_23 with reduced coverage and single nucleotide polymorphism density in both male morphs compared to females. Within this sex region, distinct Y-haplotypes delineate the two male morphs, and candidate genes for body size (GHRHR, a known dwarfism gene) and sex determination (ADCYAP1R1) are in high linkage disequilibrium. Because differences in body size between females and males are under strong selection in L.callipterus, we hypothesize that sexual antagonism over body size initiated early events in sex chromosome evolution, followed by Y divergence to give rise to bourgeois and dwarf male reproductive strategies. Our results are consistent with the hypothesis that sexually antagonistic traits should be linked to young sex chromosomes.

Individual territoriality in lekking species: the case of the Helmeted Manakin

ABSTRACT Neotropical manakins exhibit polygynous lekking systems in which males do not provide paternal care and exhibit elaborate courtship displays. Despite familial patterns, some historical field observations suggested that the Helmeted Manakin (Antilophia galeata) has evolved territoriality rather than lekking and a socially monogamous mating system. Furthermore, the evidence so far does not allow a clear understanding of the role played by resources, such as nesting sites and male behaviour in shaping the mating system in this species. Our objectives were to verify whether territorial behaviour occurs in the Helmeted Manakin and to provide a preliminary assessment of this species’ hypothesised social monogamy. Using an experimental approach with simulated territorial intrusions, we demonstrated that males in this species hold individual territories with nesting sites but do not provide parental care, similar to its congener, the Araripe Manakin (Antilophia bokermanni). Males’ responses occurred more aggressively in central areas of territories. Larger home ranges encompassed the smaller defended territories and the male display consists of repeated circular flights within the territory. Our results indicate that the Helmeted Manakin has a polygamous mating system. However, we suggest the species is better classified within the continuum of a resource-defence exploded-lek mating system. The distinct environmental conditions in which the species evolved may have played a significant role in modifying its behaviour, resulting in patterns that deviate from the typical lekking system found among manakins. This study highlights the importance of investigating atypical manakins to further our understanding of alternative reproductive tactics among birds.