Kin-mediated plasticity in alternative reproductive tactics.

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.

The role of genetic diversity in the evolution and maintenance of environmentally-cued, male alternative reproductive tactics.

BACKGROUND: Alternative reproductive tactics (ARTs) are taxonomically pervasive strategies adopted by individuals to maximize reproductive success within populations. Even for conditionally-dependent traits, consensus postulates most ARTs involve both genetic and environmental interactions (GEIs), but to date, quantifying genetic variation underlying the threshold disposing an individual to switch phenotypes in response to an environmental cue has been a difficult undertaking. Our study aims to investigate the origins and maintenance of ARTs within environmentally disparate populations of the microscopic bulb mite, Rhizoglyphus robini, that express 'fighter' and 'scrambler' male morphs mediated by a complex combination of environmental and genetic factors. RESULTS: Using never-before-published individual genetic profiling, we found all individuals across populations are highly inbred with the exception of scrambler males in stressed environments. In fact within the poor environment, scrambler males and females showed no significant difference in genetic differentiation (Fst) compared to all other comparisons, and although fighters were highly divergent from the rest of the population in both poor or rich environments (e.g., Fst, STRUCTURE), fighters demonstrated approximately three times less genetic divergence from the population in poor environments. AMOVA analyses further corroborated significant genetic differentiation across subpopulations, between morphs and sexes, and among subpopulations within each environment. CONCLUSION: Our study provides new insights into the origin of ARTs in the bulb mite, highlighting the importance of GEIs: genetic correlations, epistatic interactions, and sex-specific inbreeding depression across environmental stressors. Asymmetric reproductive output, coupled with the purging of highly inbred individuals during environmental oscillations, also facilitates genetic variation within populations, despite evidence for strong directional selection. This cryptic genetic variation also conceivably facilitates stable population persistence even in the face of spatially or temporally unstable environmental challenges. Ultimately, understanding the genetic context that maintains thresholds, even for conditionally-dependent ARTs, will enhance our understanding of within population variation and our ability to predict responses to selection.

Fitness consequences of threshold trait expression subject to environmental cues.

Most cases of alternative reproductive tactics (ARTs) are thought to represent conditional strategies, whereby high-status males express highly competitive phenotypes, whereas males below a certain status threshold resort to sneaky tactics. The underlying evolutionarily stable strategy (ESS) model assumes that males of high competitive ability achieve higher fitness when expressing the territorial phenotype, whereas the less competitive males are more fit as sneakers, caused by fitness functions for the ARTs having different slopes and intersecting at a threshold value of competitive ability. The model, however, is notoriously difficult to test as it requires access to low-status territorials and high-status sneakers, that rarely occur in nature. Here, we test the conditional ESS in the androdimorphic acarid mite Sancassania berlesei, where large males tend to develop into an armoured, aggressive 'fighter' morph, while small males become unarmoured, non-aggressive 'scramblers'. In addition to body size, male morph is affected by pheromones produced by big populations, with fighters being suppressed in dense colonies. By manipulating pheromone concentration, we obtained high-status scramblers and low-status fighters. We also estimated status- and size-dependent fitness functions for male morphs across a range of population sizes. Fighters had the highest fitness in small populations and their fitness declined with increasing density, whereas the reverse was true for scramblers, providing support for condition-dependent ESS with respect to demography. However, whereas male fitness increased with body size, the fitness functions did not differ significantly between morphs. Thus, although we found evidence for the intersection of morph fitness functions with respect to demography, we did not find such an intersection in relation to male body size. Our results highlight how demography can exert selection pressures shaping the evolution of the conditional strategy in species with ARTs.

Morph-specific artificial selection reveals a constraint on the evolution of polyphenisms.

Theory predicts that the evolution of polyphenic variation is facilitated where morphs are genetically uncoupled and free to evolve towards their phenotypic optima. However, the assumption that developmentally plastic morphs can evolve independently has not been tested directly. Using morph-specific artificial selection, we investigated correlated evolution between the sexes and male morphs of the bulb mite Rhizoglyphus echinopus Large 'fighter' males have a thick and sharply terminating pair of legs used to kill rival males, while small 'scrambler' males have unmodified legs, and search for unguarded females, avoiding fights. We selected on the relative leg width of only the fighter male morph, tracked the evolutionary responses in fighters and the correlated evolutionary responses in scramblers and females that were untouched by direct selection. Fighters diverged in relative leg thickness after six generations; assaying scramblers and females at the ninth generation we observed correlated responses in relative leg width in both. Our results represent strong evidence for the evolution of intraspecific phenotypic diversity despite correlated evolution between morphs and sexes, challenging the idea that male morphs are genetically uncoupled and free to independently respond to selection. We therefore question the perceived necessity for genetic independence in traits with extreme phenotypic plasticity.

Be a good loser: A theoretical model for subordinate decision-making on bi-directional sex change in haremic fishes.

Among animals living in groups with reproductive skew associated with a dominance hierarchy, subordinates may do best by using various alternative tactics. Sequential hermaphrodites or sex changers adopt a unique solution, that is, being the sex with weaker skew when they are small and subordinate, and changing sex when they become larger. In bi-directionally sex-changing fishes, although most are haremic and basically protogynous, subordinate males can change sex to being females. We study a mathematical model to examine when and why such reversed sex change is more adaptive than dispersal to take over another harem. We attempt to examine previously proposed hypotheses that the risk of dispersal and low density favor reversed sex change, and to specify an optimal decision-making strategy for subordinates. As a result, while the size-dependent conditional strategy in which smaller males tend to change sex is predicted, even large males are predicted to change sex under low density and/or high risk of dispersal, supporting both previous hypotheses. The importance of spatiotemporal variation of social and ecological conditions is also suggested. We discuss a unified framework to understand hermaphroditic and gonochoristic societies.

A model for conditional male trimorphisms.

Conditional dimorphisms are widespread in color, morphology, behavior, and life history. Such traits have been successfully modeled in game theory as conditional strategies, and in quantitative genetics as threshold traits. Conditional trimorphisms have recently been unveiled, and here we combine the rock-paper-scissors (RPS) model of game theory and the environmental threshold (ET) model of quantitative genetics to model trimorphisms that are environmentally induced and result from the expression of two thresholds. We investigated the tactic fitness structure for maintenance of alternative reproductive tactics in scarab dung beetles that constitute the first known examples of conditional male trimorphism. We parameterized a novel ternary fitness landscape that explains how conditional male trimorphism in these beetles can be maintained. We tracked changes in tactic frequencies in a wild population of Phanaeus triangularis and detected fitness intransitivity consistent with RPS dynamics. Quantitative predictions of our model compare favorably with corresponding observed parameters. The ternary landscape further reveals how geographic populations of these beetles can evolve between conditional trimorphism and dimorphism. The ternary model also suggests that polyphenic systems could potentially evolve between conditional and purely genetic mediation.

Absolute versus Relative Assessments of Individual Status in Status-Dependent Strategies in Stochastic Environments.

Status-dependent strategies represent one of the most remarkable adaptive phenotypic plasticities. A threshold value for individual status (e.g., body size) is assumed above and below which each individual should adopt alternative tactics to attain higher fitness. This implicitly assumes the existence of an "absolute" best threshold value, so each individual chooses a tactic only on the basis of its own status. However, animals may be able to assess their status on the basis of surrounding individuals. This "relative" assessment considers a threshold value to be changeable depending on individual situations, which may result in significant differences in ecological and evolutionary dynamics compared with absolute assessment. Here, we incorporated Bayesian decision-making and adaptive dynamics frameworks to explore the conditions necessary for each type of assessment to evolve. Our model demonstrates that absolute assessment is always an evolutionarily stable strategy (ESS) in a stable environment, whereas relative assessment can be an ESS in stochastic environments. The consequences of future environmental change differ considerably depending on the assessment chosen. Our results underscore the need to better understand how individuals assess their own status when choosing alternative tactics.

Shifting Thresholds: Rapid Evolution of Migratory Life Histories in Steelhead/Rainbow Trout, Oncorhynchus mykiss.

Expression of phenotypic plasticity depends on reaction norms adapted to historic selective regimes; anthropogenic changes in these selection regimes necessitate contemporary evolution or declines in productivity and possibly extinction. Adaptation of conditional strategies following a change in the selection regime requires evolution of either the environmentally influenced cue (e.g., size-at-age) or the state (e.g., size threshold) at which an individual switches between alternative tactics. Using a population of steelhead (Oncorhynchus mykiss) introduced above a barrier waterfall in 1910, we evaluate how the conditional strategy to migrate evolves in response to selection against migration. We created 9 families and 917 offspring from 14 parents collected from the above- and below-barrier populations. After 1 year of common garden-rearing above-barrier offspring were 11% smaller and 32% lighter than below-barrier offspring. Using a novel analytical approach, we estimate that the mean size at which above-barrier fish switch between the resident and migrant tactic is 43% larger than below-barrier fish. As a result, above-barrier fish were 26% less likely to express the migratory tactic. Our results demonstrate how rapid and opposing changes in size-at-age and threshold size contribute to the contemporary evolution of a conditional strategy and indicate that migratory barriers may elicit rapid evolution toward the resident life history on timescales relevant for conservation and management of conditionally migratory species.

Intralocus tactical conflict: genetic correlations between fighters and sneakers of the dung beetle Onthophagus taurus.

Males and females differ in their phenotypic optima for many traits, and as the majority of genes are expressed in both sexes, some alleles can be beneficial to one sex but harmful to the other (intralocus sexual conflict; ISC). ISC theory has recently been extended to intrasexual dimorphisms, where certain alleles may have opposite effects on the fitness of males of different morphs that employ alternative reproductive tactics (intralocus tactical conflict; ITC). Here, we use a half-sib breeding design to investigate the genetic basis for ISC and ITC in the dung beetle Onthophagus taurus. We found positive heritabilities and intersexual genetic correlations for almost all traits investigated. Next, we calculated the intrasexual genetic correlation between males of different morphs for horn length, a sexually selected trait, and compared it to intrasexual correlations for naturally selected traits in both sexes. Intrasexual genetic correlations did not differ significantly between the sexes or between naturally and sexually selected traits, failing to support the hypothesis that horns present a reduction of intrasexual genetic correlations due to ITC. We discuss the implications for the idea of developmental reprogramming between male morphs and emphasize the importance of genetic correlations as constraints for the evolution of dimorphisms.

Toward an understanding of the chemical ecology of alternative reproductive tactics in the bulb mite (Rhizoglyphus robini).

BACKGROUND: Under strong sexual selection, certain species evolve distinct intrasexual, alternative reproductive tactics (ARTs). In many cases, ARTs can be viewed as environmentally-cued threshold traits, such that ARTs coexist if their relative fitness alternates over the environmental cue gradient. Surprisingly, the chemical ecology of ARTs has been underexplored in this context. To our knowledge, no prior study has directly quantified pheromone production for ARTs in a male-polymorphic species. Here, we used the bulb mite-in which males are either armed fighters that kill conspecifics, or unarmed scramblers (which have occasionally been observed to induce mating behavior in other males)-as a model system to gain insight into the role of pheromones in the evolutionary maintenance of ARTs. Given that scramblers forgo investment into weaponry, we tested whether scramblers produce higher quantities of the putative female sex-pheromone α-acaridial than fighters, which would improve the fitness of the scrambler phenotype through female mimicry by allowing avoidance of aggression from competitors. To this end, we sampled mites from a rich and a poor nutritional environment and quantified their production of α-acaridial through gas chromatography analysis. RESULTS: We found a positive relationship between pheromone production and body size, but males exhibited a steeper slope in pheromone production with increasing size than females. Females exhibited a higher average pheromone production than males. We found no significant difference in slope of pheromone production over body size between fighters and scramblers. However, scramblers reached larger body sizes and higher pheromone production than fighters, providing some evidence for a potential female mimic strategy adopted by large scramblers. Pheromone production was significantly higher in mites from the rich nutritional environment than the poor environment. CONCLUSION: Further elucidation of pheromone functionality in bulb mites, and additional inter- and intrasexual comparisons of pheromone profiles are needed to determine if the observed intersexual and intrasexual differences in pheromone production are adaptive, if they are a by-product of allometric scaling, or diet-mediated pheromone production under weak selection. We argue chemical ecology offers a novel perspective for research on ARTs and other complex life-history traits.

Behavioral plasticity and G × E of reproductive tactics in Nicrophorus vespilloides burying beetles.

Phenotypic plasticity is important in the evolution of traits and facilitates adaptation to rapid environmental changes. However, variation in plasticity at the individual level, and the heritable basis underlying this plasticity is rarely quantified for behavioral traits. Alternative behavioral reproductive tactics are key components of mating systems but are not often considered within a phenotypic plasticity framework (i.e., as reaction norms). Here, using lines artificially selected for repeated mating rate, we test for genetic (G × E) sources of variation in reproductive behavior of male Nicrophorus vespilloides burying beetles (including signaling behavior), as well as the role of individual body size, in responsiveness to changes in social environment. The results show that body size influences the response of individuals' signaling behavior to changes in the social environment. Moreover, there was G × E underlying the responses of males to variation in the quality of social environment experienced (relative size of focal male compared to his rival). This shows that individual variation in plasticity and social sensitivity of signaling behavior can evolve in response to selection on investment in mating behavior, with males selected for high mating investment having greater social sensitivity.

Good for the group? Explaining apparent group-level adaptation.

The idea that group selection can explain adaptive trait evolution is still controversial. Recent empirical work proposes evidence for group-level adaptation in a social spider, but the findings can also be explained from an individual-level perspective. The challenge remains to identify situations where one can separate group and individual selection.

Colony size, but not density, affects survival and mating success of alternative male reproductive tactics in a polyphenic mite, Rhizoglyphus echinopus.

Among acarid mites, a number of species are characterised by the presence of discontinuous morphologies (armed heteromorphs vs. unarmed homeomorphs) associated with alternative mating tactics (fighting vs. scramble competition). In Rhizoglyphus echinopus, expression of the fighter morph is suppressed, via pheromones, in large, dense colonies. If this mechanism is adaptive, fighters should have relatively lower fitness in large and/or dense colonies, due to costs incurred from fighting, which is often fatal. In order to test these predictions, we quantified the survival and mating success of fighters and scramblers in colonies of equal sex and morph ratios; these colonies either differed in size (4, 8, or 32 individuals) but not density or differed in density but not size (all consisted of 8 individuals). We found that the relative survival and mating success of fighters was inversely related to colony size, but we did not find a significant effect of colony density. The higher mating success of fighters in small colonies was due to the fact that, after killing rival males, these fighters were able to monopolise females. This situation was not found in larger colonies, in which there was a larger number of competitors and fighters suffered relatively higher mortality. These results indicate that morph determination, guided by social cues, allows for the adaptive adjustment of mating tactics to existing demographic conditions.