Genetic correlations across genetically determined and developmentally plastic alternative reproductive tactics

AbstractAlternative reproductive tactics occur when individuals of the same sex have a suite of morphological and/or behavioural traits that allow them to pursue different reproductive strategies. A common pattern is e.g. the existence of “courter” and “sneaker” tactics within males. We have previously argued that alternative reproductive tactics should be subject to genetic conflict over the phenotypic expression of traits, similar to sexual antagonism. In this process, which we called intra-locus tactical conflict, genetically determined tactics experience conflicting selection on a shared phenotypic trait, such as body size, but a positive genetic correlation between tactics in body size prevents either tactic from reaching its optimum. Recently, other authors have attempted to extend this idea to developmentally plastic alternative reproductive tactics, with mixed results. However, it is not clear whether we should expect intra-locus tactical conflict in developmentally plastic tactics or not. We have therefore run a series of simulation models investigating under what conditions we should expect to see positive estimates of the inter-tactical genetic correlation, since a positive genetic correlation is a prerequisite for the existence of intra-locus tactical conflict. We found that for autosomal, X-linked, and Y-linked genetically-determined tactics, estimated inter-tactical genetic correlations were generally high. However, for developmentally plastic tactics, the genetic correlation depends on the properties of the switching threshold between tactics. If it is fixed, then estimated genetic correlations are positive, but if there is genetic variation in the switch-point, then any sign and magnitude of estimated genetic correlation is possible, even for highly heritable traits where the true underlying correlation is perfect. This means that caution should be used when investigating genetic constraints in plastic phenotypes.

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The evolution of genetic and conditional alternative reproductive tactics

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.2945 ◽

2016 ◽

Vol 283 (1825) ◽

pp. 20152945 ◽

Cited By ~ 27

Author(s):

Leif Engqvist ◽

Michael Taborsky

Keyword(s):

Body Size ◽

Size Variation ◽

Alternative Reproductive Tactics ◽

Disruptive Selection ◽

Relevant Parameter ◽

Reproductive Tactics ◽

Adaptive Diversification ◽

Size Dependent ◽

Mortality Causes ◽

Genetically Determined

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.

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Evidence for tactically antagonistic selection on body size and the sword in a wild population of the swordtail fish, Xiphophorus multilineatus

10.22541/au.160875615.53047765/v1 ◽

2020 ◽

Author(s):

Melissa Liotta ◽

Jessica Abbott ◽

Molly Morris ◽

Oscar Rios-Cardenas

Keyword(s):

Body Size ◽

Body Shape ◽

Behavioral Plasticity ◽

Wild Population ◽

Copulatory Behavior ◽

Alternative Reproductive Tactics ◽

Reproductive Tactics ◽

Genetic Conflict ◽

Antagonistic Selection ◽

Selection Gradients

Intralocus conflict has been well documented between the sexes, but much less is known about the potential for this genetic conflict in other polymorphisms, such as alternative reproductive tactics. Here we investigate two of three criteria necessary for demonstrating intralocus tactical conflict: the ARTs have different phenotypic optima for a shared trait, and one or both ARTs are not at their phenotypic optima for a shared trait. We address these two criteria in Xiphophorus multilineatus, a live-bearing freshwater fish that has two male alternative reproductive tactics, a behaviorally fixed courter male and a behaviorally plastic sneaker male that switches between courtship and force-copulatory behavior. We used measures of reproductive success from a wild population to estimate selection gradients on three tactically dimorphic traits involved in sexual selection: body size, body shape, and sword length. We present evidence that both body size and sword length are experiencing tactically antagonistic selection, providing evidence for both criteria. Additionally, selection on body shape in sneaker males appears to be buffered due to behavioral plasticity. Our study provides novel insight from a wild population into the role that intralocus tactical conflict can play in constraining ARTs from reaching their respective phenotypic optima despite tactical dimorphism.

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Alternative Reproductive Tactics

Reproductive Biology ◽

10.1093/oso/9780190688554.003.0015 ◽

2020 ◽

pp. 429-446

Author(s):

Shawn Garner ◽

Bryan Neff

Keyword(s):

Body Size ◽

Small Body ◽

Large Body ◽

Morphological Differentiation ◽

Alternative Reproductive Tactics ◽

Reproductive Tactics ◽

Aggressive Interactions ◽

Single Sex ◽

Female Mimicry ◽

Mating Opportunities

Alternative reproductive tactics (ARTs) describe variation among individuals of a single sex in the tactics used to obtain mating opportunities. In crustaceans, ARTs have been observed in multiple taxa and take a variety of forms. ARTs are most commonly observed in males and are generally associated with intense competition among males to monopolize access to breeding females. ARTs frequently involve a guard tactic that competes with other males to monopolize access to females, while a second usurper tactic foregos competition with other males and instead obtains mating opportunities through sneaking behavior. Guard and usurper tactics may be expressed conditionally based on a male’s ability to guard a female (e.g. his body size, the abundance of competitors), or may be expressed as discrete phenotypes that can also include morphological differentiation. For example, in Jassa amphipods the guard tactic is associated with large body size and an enlarged “thumb” on the claw that is used in aggressive interactions with other males, while the usurper tactic is associated with small body size and a reduced thumb. The usurper tactic can take two forms in a marine isopod: small males (gamma) use sneaking behavior to avoid competition with large males (alpha), whereas intermediate-sized males (beta) use female mimicry to avoid competition. Overall, ARTs are well-represented in crustaceans, with many opportunities for continued study to better characterize these unique adaptations.

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

10.21203/rs.3.rs-677523/v1 ◽

2021 ◽

Author(s):

Adam N. Zeeman ◽

Isabel M. Smallegange ◽

Emily Burdfield Steel ◽

Astrid T. Groot ◽

Kathryn A. Stewart

Keyword(s):

Body Size ◽

Chemical Ecology ◽

Alternative Reproductive Tactics ◽

Relative Fitness ◽

Pheromone Production ◽

Reproductive Tactics ◽

Female Mimicry ◽

Significant Difference ◽

Nutritional Environment ◽

Bulb Mite

Abstract BackgroundUnder 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—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 pheromone quantities than fighters, which would improve the fitness of the scrambler phenotype, e.g. through female mimicry to avoid aggression from competitors. To this end, we sampled mites from a rich and a poor nutritional environment and quantified their production of the female sex pheromone α-acaridial through gas chromatography analysis. ResultsWe 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. ConclusionFurther 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.

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

10.1101/528703 ◽

2019 ◽

Author(s):

KA Stewart ◽

R Draaijer ◽

MR Kolasa ◽

IM Smallegange

Keyword(s):

Genetic Variation ◽

Genetic Differentiation ◽

Genetic Correlations ◽

Alternative Reproductive Tactics ◽

Population Variation ◽

Reproductive Tactics ◽

Genetic Profiling ◽

Significant Difference ◽

The Face ◽

Bulb Mite

AbstractBackgroundAlternative 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.ResultsUsing 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.ConclusionOur 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.

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Environmental Influence on Life-History Traits in Male Squid Uroteuthis Edulis With Alternative Reproductive Tactics

10.21203/rs.3.rs-1002647/v1 ◽

2021 ◽

Author(s):

Yumeng Pang ◽

Chih-Shin Chen ◽

Tomohiko Kawamura ◽

Yoko Iwata

Keyword(s):

Life History ◽

Body Size ◽

Growth Rates ◽

Life History Traits ◽

Environmental Influence ◽

Life Stage ◽

Energy Allocation ◽

Alternative Reproductive Tactics ◽

Reproductive Tactics ◽

Somatic Energy

Abstract Squid are characterized by flexible life-history traits (LHTs) that change in response to changing oceanic parameters. Male alternative reproductive tactics (ARTs), characterized by large-sized ‘consorts’ versus small-sized ‘sneakers’, are commonly observed in loliginid species. This study reports on LHTs flexibility in male squids displaying ARTs. LHTs of consorts and sneakers in Uroteuthis edulis, including body size, age, growth rate and gonado-somatic energy allocation, were compared among seasonal and geographical groups from Japan and Taiwan. The ratio of consorts to sneakers was highest in the group spawning in the ‘Japan-warm’ season (June-November), followed by that of the ‘Japan-cold’ season (December-May), and lowest in Taiwan (spring and autumn). LHTs were compared among cohorts separated by hatching season and catch location (Jwarm, Jcold and Taiwan cohorts). Mean body size of consorts showed no difference among cohorts, although Taiwan consorts were relatively younger than Japan consorts. Mean size and age of sneakers decreased with increased water temperature at hatching. Growth rates of consorts and sneakers were slightly different among cohorts, in accordance with differences of statolith increment widths during their early life stage (50-150 d). Growth rates of both consorts and sneakers were highest in the Taiwan cohort, followed by the Jwarm cohort, with the Jcold cohort lowest. Sneakers invested more both in mantle and gonadal weights than consorts in all cohorts. Gonado-somatic energy allocation patterns of consorts and sneakers were consistent at different temperatures. LHTs of U. edulis consorts and sneakers were strongly influenced by temperature, with higher flexibility in sneakers than consorts.

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Antagonistic selection on body size and sword length in a wild population of the swordtail fish, Xiphophorus multilineatus: potential for intralocus tactical conflict

10.22541/au.160875615.53047765/v2 ◽

2021 ◽

Author(s):

Melissa Liotta ◽

Jessica Abbott ◽

Molly Morris ◽

Oscar Rios-Cardenas

Keyword(s):

Sexual Selection ◽

Body Size ◽

Wild Population ◽

Genetic Correlations ◽

Reproductive Tactics ◽

Swordtail Fish ◽

The Arts ◽

In The Wild ◽

Life History Tradeoffs

Alternative reproductive tactics (ARTs) have provided valuable insights into how sexual selection and life history tradeoffs can lead to variation within a sex. However, the possibility that tactics may constrain evolution through intralocus tactical conflict (IATC) is rarely considered. In addition, when IATC has been considered, the focus has often been on the genetic correlations between the ARTs, while evidence that the ARTs have different optima for associated traits and that at least one of the tactics is not at its optima is often missing. Here we investigate selection on three traits associated with the ARTs in the swordtail fish Xiphophorus multilineatus; body size, body shape and the sexually selected trait for which these fishes were named, sword length (elongation of the caudal fin). All three traits are tactically dimorphic, with courter males being larger, deeper bodied and having longer swords, and the sneaker males being smaller, more fusiform and having shorter swords. Using measures of reproductive success in a wild population we calculated selection differentials, linear and quadratic gradients, demonstrate that the tactics have different optima and at least one of the tactics is not at its optima for body size and sword length. Our results provide the first evidence of selection in the wild on the sword, an iconic trait for sexual selection. In addition, given the high probability that these traits are genetically correlated to some extent between the two tactics, our study suggests that IATC is constraining both body size and the sword from reaching their phenotypic optima. We discuss the importance of considering the role of IATC in the evolution of tactical dimorphism, how this conflict can be present despite tactical dimorphism, and how it is important to consider this conflict when explaining not only variation within a species but differences across species as well.

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Interhemispheric Relationship of Genetic Influence on Human Brain Connectivity

Cerebral Cortex ◽

10.1093/cercor/bhaa207 ◽

2020 ◽

Vol 31 (1) ◽

pp. 77-88

Author(s):

Suyu Zhong ◽

Long Wei ◽

Chenxi Zhao ◽

Liyuan Yang ◽

Zengru Di ◽

...

Keyword(s):

Human Brain ◽

Genetic Correlation ◽

Genetic Factors ◽

Brain Connectivity ◽

Genetic Correlations ◽

Disease States ◽

Left And Right ◽

Genetically Determined ◽

Relationship Of ◽

Insight Into

Abstract To understand the origins of interhemispheric differences and commonalities/coupling in human brain wiring, it is crucial to determine how homologous interregional connectivities of the left and right hemispheres are genetically determined and related. To address this, in the present study, we analyzed human twin and pedigree samples with high-quality diffusion magnetic resonance imaging tractography and estimated the heritability and genetic correlation of homologous left and right white matter (WM) connections. The results showed that the heritability of WM connectivity was similar and coupled between the 2 hemispheres and that the degree of overlap in genetic factors underlying homologous WM connectivity (i.e., interhemispheric genetic correlation) varied substantially across the human brain: from complete overlap to complete nonoverlap. Particularly, the heritability was significantly stronger and the chance of interhemispheric complete overlap in genetic factors was higher in subcortical WM connections than in cortical WM connections. In addition, the heritability and interhemispheric genetic correlations were stronger for long-range connections than for short-range connections. These findings highlight the determinants of the genetics underlying WM connectivity and its interhemispheric relationships, and provide insight into genetic basis of WM connectivity asymmetries in both healthy and disease states.

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

BMC Ecology and Evolution ◽

10.1186/s12862-021-01956-w ◽

2022 ◽

Vol 22 (1) ◽

Author(s):

Adam N. Zeeman ◽

Isabel M. Smallegange ◽

Emily Burdfield Steel ◽

Astrid T. Groot ◽

Kathryn A. Stewart

Keyword(s):

Body Size ◽

Chemical Ecology ◽

Alternative Reproductive Tactics ◽

Relative Fitness ◽

Pheromone Production ◽

Reproductive Tactics ◽

Female Mimicry ◽

Significant Difference ◽

Nutritional Environment ◽

Bulb Mite

Abstract 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.

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Intralocus sexual conflict can maintain alternative reproductive tactics

10.1101/2021.11.26.470147 ◽

2021 ◽

Author(s):

Madilyn Marisa Gamble ◽

Ryan G Calsbeek

Keyword(s):

Sexual Conflict ◽

Genetic Correlations ◽

Alternative Reproductive Tactics ◽

Specific Gene ◽

Reproductive Tactics ◽

Frequency Dependent ◽

Frequency Dependent Selection ◽

Intralocus Sexual Conflict ◽

Maintenance Of Sex ◽

Negative Frequency Dependent Selection

Alternative reproductive tactics (ARTs) are ubiquitous throughout the animal kingdom and widely regarded as an outcome of high variance in reproductive success. Proximate mechanisms underlying ARTs include genetically based polymorphisms, environmentally induced polymorphisms, and those mediated by a combination of genetic and environmental factors. However, few ultimate mechanisms have been proposed to explain the maintenance of ARTs over time, the most important of which have been disruptive and negative frequency-dependent selection. Here we explore the role that intralocus sexual conflict may play in the maintenance of sex-specific ARTs. We use a genetically explicit individual-based model in which body size influences both female fecundity and male tactic through a shared genetic architecture. By modeling ART maintenance under varying selection regimes and levels of sex-specific gene expression, we explore the conditions under which intralocus sexual conflict can maintain a hypothetical ART defined by larger (alpha) and smaller (beta) tactics. Our models consistently revealed that sexual conflict can result in the persistence of a sex-specific polymorphism over hundreds of generations, even in the absence of negative frequency-dependent selection. ARTs were maintained through correlated selection when one male ART has lower fitness but produces daughters with higher fitness. These results highlight the importance of understanding selection on both sexes when attempting to explain the maintenance of ARTs. Our results are consistent with a growing literature documenting genetic correlations between male ARTs and female fitness, suggesting that the maintenance of sex-specific ARTs through intralocus sexual conflict may be common and widespread in nature.

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