Sperm and alternative reproductive tactics: a review of existing theory and empirical data.
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ABSTRACT:
SUBMITTER: Kustra MC
PROVIDER: S-EPMC7661440 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:In species with alternative reproductive tactics, there is much empirical support that parasitically spawning males have larger testes and greater sperm numbers as an evolved response to a higher degree of sperm competition, but support for higher sperm performance (motility, longevity and speed) by such males is inconsistent. We used the sand goby (Pomatoschistus minutus) to test whether sperm performance differed between breeding-coloured males (small testes, large mucus-filled sperm-duct glands; build nests lined with sperm-containing mucus, provide care) and parasitic sneaker-morph males (no breeding colouration, large testes, rudimentary sperm-duct glands; no nest, no care). We compared motility (per cent motile sperm), velocity, longevity of sperm, gene expression of testes and sperm morphometrics between the two morphs. We also tested if sperm-duct gland contents affected sperm performance. We found a clear difference in gene expression of testes between the male morphs with 109 transcripts differentially expressed between the morphs. Notably, several mucin genes were upregulated in breeding-coloured males and two ATP-related genes were upregulated in sneaker-morph males. There was a partial evidence of higher sperm velocity in sneaker-morph males, but no difference in sperm motility. Presence of sperm-duct gland contents significantly increased sperm velocity, and nonsignificantly tended to increase sperm motility, but equally so for the two morphs. The sand goby has remarkably long-lived sperm, with only small or no decline in motility and velocity over time (5 min vs. 22 h), but again, this was equally true for both morphs. Sperm length (head, flagella, total and flagella-to-head ratio) did not differ between morphs and did not correlate with sperm velocity for either morph. Thus, other than a clear difference in testes gene expression, we found only modest differences between the two male morphs, confirming previous findings that increased sperm performance as an adaptation to sperm competition is not a primary target of evolution.
| S-EPMC9923495 | biostudies-literature
Project description: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.
| S-EPMC11291626 | biostudies-literature
Project description:Conditional strategies occur when the relative fitness pay-off from expressing a given phenotype is contingent upon environmental circumstances. This conditional strategy model underlies cases of alternative reproductive tactics, in which individuals of one sex employ different means to obtain reproduction. How kin structure affects the expression of alternative reproductive tactics remains unexplored. We address this using the mite Rhizoglyphus echinopus, in which large males develop into aggressive 'fighters' and small males develop into non-aggressive 'scramblers.' Because only fighters kill their rivals, they should incur a greater indirect fitness cost when competing with their relatives, and thus fighter expression could be reduced in the presence of relatives. We raised mites in full-sibling or mixed-sibship groups and found that fighters were more common at higher body weights in full-sibling groups, not less common as we predicted (small individuals were almost exclusively scramblers in both treatments). This result could be explained if relatedness and cue variability are interpreted signals of population density, since fighters are more common at low densities in this species. Alternatively, our results may indicate that males compete more intensely with relatives in this species. We provide the first evidence of kin-mediated plasticity in the expression of alternative reproductive tactics.
| S-EPMC8334832 | biostudies-literature
Project description:Abstract During male–male competition, evolution can favor alternative reproductive tactics. This often results in a dominant morph that holds a resource, such as a nest for egg laying, which competes with a smaller sneaker morph that reproduces by stealing fertilizations. The salinity environment can influence male growth rates, for example, via osmoregulatory costs, which in turn may influence the use of sneaker tactics for small males competing for mating opportunities. Salinity can also affect sperm directly; however, little is known of how salinity influences sneaker tactics through sperm performance. We sampled males of the invasive round goby (Neogobius melanostomus) from two environments, a freshwater river and a brackish estuary. This fish has two male morphs: nest?holding dark males and non?nest?holding light males. We examined the role of water salinity of 0, 8, and 16 on sperm performance and found that for estuarine males, a salinity of 0 reduced sperm velocity compared to a salinity of 8 and 16. Riverine males had low velocity in all salinities. Sperm viability also decreased by over 30% in 0 salinity, compared to 8 and 16, for fish from both environments. Gobies produce ejaculate contents in specialized glands that could in theory shield sperm in an adverse environment. However, gland contents did not improve sperm performance in our tests. Body mass and age estimates indicate that riverine males invested more in somatic growth compared to estuarine males. Estuarine light morph males had a high enough gonadosomatic index to indicate sneaker tactics. We propose that when sperm performance is low, such as for the riverine males, sneaker tactics are ineffective and will be selected against or phenotypically suppressed. Instead, we interpret the increased investment in somatic growth found in riverine males as a life?history decision that is advantageous when defending a nest in the next reproductive season. For a male fish too small to defend mating resources such as a female or her eggs, siring offspring can be achieved by sneaking into another male's nest and ejaculating there. In the invasive round goby, this alternative tactic requires sperm to function long enough to fertilize the eggs. This fish has spread into a range of salinities, but for some populations, fresh water decreases sperm velocity and lifespan, and severely limits the use of these alternative reproductive tactics to the point where they may disappear from use.
| S-EPMC7520214 | biostudies-literature
Project description:Alternative reproductive tactics (ARTs), discrete phenotypic variations evolved to maximize fitness, may entail different cost-benefit trade-offs. In large mammals, differences in costs associated with ARTs-including energy expenditure and parasite infection-are typically greatest during the breeding season. Nonetheless, physiological and behavioral differences between ARTs can manifest throughout the year, possibly involving costs that may contribute to maintain ARTs within populations. Using the number of nematode larvae per gram of feces (LPG) as a proxy, we explored the temporal changes in lung parasite infection in territorial and nonterritorial male chamois Rupicapra in the Gran Paradiso National Park (Italy), between 2011 and 2012. We aimed to identify which tactic-specific physiological and behavioral features (including age, hormonal levels, inter- and intrasexual interactions, and space use) or climatic factors (temperature and precipitation) best explained yearly variation in parasite infection within and between ARTs. Generalized additive mixed models showed that the fecal larval counts of lung nematodes underwent strong temporal changes in both male types. Differences between ARTs (with higher LPG values in territorial than nonterritorial males) were greatest during the rut and-to a lesser extent-in spring, respectively, at the peak and at the onset of territoriality. The difference in LPG between tactics was largely explained by the greater levels of hormone metabolites in territorial males during the rut. The other variables did not contribute significantly to explain the different shedding of larvae within and between ARTs. Our analysis suggests that different values of LPG between territorial and nonterritorial males are largely a result of tactic-specific differences in the secretion of hormone metabolites, but only during the rut. To clarify whether rut-related parasitism contributes to the maintenance of ARTs, tactic-specific life history trade-offs, for example, between reproduction and parasite-related mortality, must be investigated.
| S-EPMC6686307 | biostudies-literature
Project description:Frequency-dependent selection may drive adaptive diversification within species. It is yet unclear why the occurrence of alternative reproductive tactics (ARTs) is highly divergent between major animal taxa. Here we aim to clarify the environmental and social conditions favouring the evolution of intra-population variance of male reproductive phenotypes. Our results suggest that genetically determined ARTs that are fixed for life evolve when there is strong selection on body size due to size-dependent competitiveness, in combination with environmental factors reducing size benefits. The latter may result from growth costs or, more generally, from age-dependent but size-independent mortality causes. This generates disruptive selection on growth trajectories underlying tactic choice. In many parameter settings, the model also predicts ARTs to evolve that are flexible and responsive to current conditions. Interestingly, the conditions favouring the evolution of flexible tactics diverge considerably from those favouring genetic variability. Nevertheless, in a restricted but relevant parameter space, our model predicts the simultaneous emergence and maintenance of a mixture of multiple tactics, both genetically and conditionally determined. Important conditions for the emergence of ARTs include size variation of competitors, which is inherently greater in species with indeterminate growth than in taxa reproducing only after reaching their terminal body size. This is probably the reason why ARTs are more common in fishes than in other major taxa.
| S-EPMC4810835 | biostudies-literature
Project description:Loliginid squids provide a unique model system to explore male alternative reproductive tactics (ARTs) and their linkage to size, behavioral decision making, and possibly age. Large individuals fight one another and the winners form temporary consortships with females, while smaller individuals do not engage in male-male agonistic bouts but use various sneaker tactics to obtain matings, each with varying mating and fertilization success. There is substantial behavioral flexibility in most species, as smaller males can facultatively switch to the alternative consort behaviors as the behavioral context changes. These forms of ARTs can involve different: mating posture; site of spermatophore deposition; fertilization success; and sperm traits. Most of the traits of male dimorphism (both anatomical and behavioral) are consistent with traditional sexual selection theory, while others have unique features that may have evolved in response to the fertilization environment faced by each temporary or permanent male morph.
| S-EPMC6803530 | biostudies-literature
Project description:Life history theory predicts that the amount of resources allocated to reproduction should maximize an individual's lifetime reproductive success. So far, resource allocation in reproduction has been studied mainly in females. Intraspecific variation of endogenous energy storage and utilization patterns of males has received little attention, although these patterns may vary greatly between individuals pursuing alternative reproductive tactics (ARTs). ARTs are characterized by systematic variation of behavioral, physiological, and often morphological traits among same-sex conspecifics. Some individuals may rely on previously accumulated reserves, because of limited foraging opportunities during reproduction. Others may be able to continue foraging during reproduction, thus relying on reserves to a lesser extent. We therefore predicted that, if male tactics involve such divergent limitations and trade-offs within a species, ARTs should correspondingly differ in energy reserve allocation and utilization. To test this prediction, we studied short-term and long-term reserve storage patterns of males in the shell-brooding cichlid Lamprologus callipterus. In this species, bourgeois males investing in territory defense, courtship, and guarding of broods coexist with two distinct parasitic male tactics: (1) opportunistic sneaker males attempting to fertilize eggs by releasing sperm into the shell opening when a female is spawning; and (2) specialized dwarf males attempting to enter the shell past the spawning female to fertilize eggs from inside the shell. Sneaker males differed from other male types by showing the highest amount of accumulated short-term and long-term fat stores, apparently anticipating their upcoming adoption of the nest male status. In contrast, nest males depleted previously accumulated energy reserves with increasing nest holding period, as they invest heavily into costly reproductive behaviors while not taking up any food. This conforms to a capital breeder strategy. Dwarf males did not accumulate long-term fat stores at all, which they can afford due to their small behavioral effort during reproduction and their continued feeding activity, conforming to an income breeder strategy. Our data confirm that the resource storage patterns of males pursuing ARTs can diverge substantially, which adds to our understanding of the coexistence and maintenance of alternative reproductive patterns within species.
| S-EPMC4449759 | biostudies-literature
Project description:Corticosteroid signaling mechanisms mediate a wide range of adaptive physiological responses, including those essential to reproduction. Here, we investigated the presence and relative abundance of corticosteroid receptors during the breeding season in the plainfin midshipman fish (Porichthys notatus), a species that has two male reproductive morphs. Only type I "singing" males acoustically court females and aggressively defend a nest site, whereas type II "sneaker" males steal fertilizations from nesting type I males. Cloning and sequencing first identified glucocorticoid (GR) and mineralocorticoid (MR) receptors in midshipman that exhibited high sequence identity with other vertebrate GRs and MRs. Absolute-quantitative real-time PCR then revealed higher levels of GR in the central nervous system (CNS) of type II males than type I males and females, while GR levels in the sound-producing, vocal muscle and the liver were higher in type I males than type II males and females. MR expression was also greater in the CNS of type II males than type I males or females, but the differences were more modest in magnitude. Lastly, plasma levels of cortisol, the main glucocorticoid in teleosts, were 2- to 3-fold greater in type II males compared to type I males. Together, the results suggest a link between corticosteroid regulation and physiological and behavioral variation in a teleost fish that displays male alternative reproductive tactics.
| S-EPMC2783833 | biostudies-literature
Project description:In socially monogamous species, pair-bonded males often continue to provide care to all offspring in their nests despite some degree of paternity loss due to female extra-pair copulation. Previous theoretical models suggested that females can use their within-pair offspring as 'hostages' to blackmail their social mates, so that they continue to provide care to the brood at low levels of cuckoldry. These models, however, rely on the assumption of sufficiently accurate male detection of cuckoldry and the reduction of parental effort in case of suspicion. Therefore, they cannot explain the abundant cases where cuckolded males continue to provide extensive care to the brood. Here we use an analytical population genetics model and an individual-based simulation model to explore the coevolution of female fidelity and male help in populations with two genetically determined alternative reproductive tactics (ARTs): sneakers that achieve paternity solely via extra-pair copulations and bourgeois that form a mating pair and spend some efforts in brood care. We show that when the efficiency of mate guarding is intermediate, the bourgeois males can evolve to 'specialize' in providing care by spending more than 90% of time in helping their females while guarding them as much as possible, despite frequent cuckoldry by the sneakers. We also show that when sneakers have tactic-specific adaptations and thus are more competitive than the bourgeois in gaining extra-pair fertilizations, the frequency of sneakers and the degrees of female fidelity and male help can fluctuate in evolutionary cycles. Our theoretical predictions highlight the need for further empirical tests in species with ARTs.
| S-EPMC7893278 | biostudies-literature