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

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

10.1101/2021.06.30.450527 ◽

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

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 — 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. 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 byproduct 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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Alternative reproductive tactics and sex‐biased gene expression: the study of the bulb mite transcriptome

Ecology and Evolution ◽

10.1002/ece3.965 ◽

2014 ◽

Vol 4 (5) ◽

pp. 623-632 ◽

Cited By ~ 41

Author(s):

Michal T. Stuglik ◽

Wiesław Babik ◽

Zofia Prokop ◽

Jacek Radwan

Keyword(s):

Gene Expression ◽

Alternative Reproductive Tactics ◽

Reproductive Tactics ◽

Bulb Mite

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Genetic correlations across genetically determined and developmentally plastic alternative reproductive tactics

10.1101/768721 ◽

2019 ◽

Author(s):

Jessica K. Abbott ◽

Oscar Rios-Cardenas ◽

Molly Morris

Keyword(s):

Body Size ◽

Genetic Correlation ◽

Genetic Correlations ◽

Phenotypic Expression ◽

Alternative Reproductive Tactics ◽

Phenotypic Trait ◽

Sexual Antagonism ◽

Reproductive Tactics ◽

Genetic Conflict ◽

Genetically Determined

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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Genetic Differentiation of the Two Types of Polish Cold-blooded Horses Included in the National Conservation Program

Animals ◽

10.3390/ani10030542 ◽

2020 ◽

Vol 10 (3) ◽

pp. 542

Author(s):

Artur Gurgul ◽

Igor Jasielczuk ◽

Ewelina Semik-Gurgul ◽

Klaudia Pawlina-Tyszko ◽

Tomasz Szmatoła ◽

...

Keyword(s):

Genetic Variation ◽

Molecular Markers ◽

Genetic Differentiation ◽

Gene Pool ◽

Population Variation ◽

Horse Population ◽

Current Role ◽

Conservation Program ◽

Conservation Breeding

The current role of the horse as a companion animal resulted in a decrease of interest in breeding and usage of draft horses. This meant that the population of cold-blooded horses in Poland has been dramatically reduced during the last decades. To avoid impoverishment of the gene pool of the local horse population, a conservation program was established which involves draft horses and other local horse breeds. The draft horses bred in Poland can be subdivided in a few horse types of which the most widespread and consolidated are Sztumski and Sokólski horses. These two subpopulations are phenotypically diversified, however, the overall level of their genetic differentiation seems to be relatively low and not precisely determined, especially with the use of molecular markers. In reference to this, in this study we used Illumina genotyping arrays to describe in detail the genetic differentiation of these two cold-blooded horse populations. We describe the genetic distance between them, as well as within-population variation, admixture patterns, and level of relatedness within populations. We also made an attempt to detect genome regions divergently selected between those horses by the detection of diversifying selection signals. The results of this study provide initial evidence supporting breeding decisions that were made during conservation breeding program design and answer questions raised by the breeders of Sokólski and Sztumski horses concerning the level of their genetic variation and differentiation.

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Sperm and alternative reproductive tactics: a review of existing theory and empirical data

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0075 ◽

2020 ◽

Vol 375 (1813) ◽

pp. 20200075

Author(s):

Matthew C. Kustra ◽

Suzanne H. Alonzo

Keyword(s):

Sperm Competition ◽

Empirical Data ◽

Alternative Reproductive Tactics ◽

Theme Issue ◽

Reproductive Tactics ◽

Comprehensive Review ◽

Trade Offs ◽

Significant Difference ◽

General Expectation ◽

Sperm Traits

Males that exhibit alternative reproductive tactics (ARTs) often differ in the risk of sperm competition and the energetic trade-offs they experience. The resulting patterns of selection could lead to between-tactic differences in ejaculate traits. Despite extensive research on male ARTs, there is no comprehensive review of whether and what differences in sperm traits exist between male ARTs. We review existing theory on ejaculate evolution relevant to ARTs and then conduct a comprehensive vote-counting review of the empirical data comparing sperm traits between males adopting ARTs. Despite the general expectation that sneaker males should produce sperm that are more competitive (e.g. higher quality or performance), we find that existing theory does not predict explicitly how males adopting ARTs should differ in sperm traits. The majority of studies find no significant difference in sperm performance traits between dominant and sneaker males. However, when there is a difference, sneaker males tend to have higher sperm performance trait values than dominant males. We propose ways that future theoretical and empirical research can improve our understanding of the evolution of ejaculate traits in ARTs. We then highlight how studying ejaculate traits in species with ARTs will improve our broader knowledge of ejaculate evolution. This article is part of the theme issue ‘Fifty years of sperm competition’.

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Genetic Variation Among and Within Populations in Swedish Species of Sorbus aucuparia L. and Prunus padus L. Assessed in a Nursery Trial

Silvae Genetica ◽

10.1515/sg-2005-0001 ◽

2005 ◽

Vol 54 (1-6) ◽

pp. 1-8 ◽

Cited By ~ 12

Author(s):

V. Baliuckas ◽

T. Lagerström ◽

L. Norell ◽

G. Eriksson

Keyword(s):

Genetic Variation ◽

Growth Traits ◽

Genetic Correlations ◽

Population Variation ◽

Sorbus Aucuparia ◽

Population Effect ◽

Prunus Padus ◽

Bud Flushing ◽

Over Time ◽

Leaf Colouring

Abstract Seedlings originating from open-pollinated offspring of six and four populations of Prunus padus and Sorbus aucuparia, respectively, were studied with respect to phenology and growth traits for 3-4 years in a nursery. There were no replications at the population levels since the experiments should be converted to seedling seed orchards. Therefore, a special statistical model for analysis of the population effect was developed making use of neighbour performances. This model was also used for derivation of heritabilities. The heritabilities for phenology traits were in many cases high in P. padus, > 0.40, while they varied in the range 0.07-0.62 in S. aucuparia. The population effect was significant for all growth rhythm traits in P. padus and for a majority of traits in S. aucuparia. In both species the heritability for height decreased over time. Only bud flushing in P. padus indicated a relationship with population latitudinal origin in some cases. The genetic correlations between bud flushing different years were relatively strong in both species while the corresponding correlations for leaf colouring were moderate in P. padus and weak in S. aucuparia. In conclusion, the observed structure suggests that the pattern of seed dispersal may have an influence on the among- and within-population variation.

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Genetic Diversity among Isolates of Phytophthora sojae in Anhui Province of China based on ISSR-PCR Markers

Journal of the American Society for Horticultural Science ◽

10.21273/jashs04398-18 ◽

2018 ◽

Vol 143 (4) ◽

pp. 304-309 ◽

Cited By ~ 2

Author(s):

Dong Liu ◽

Ping Li ◽

Jiulong Hu ◽

Kunyuan Li ◽

Zhenyu Zhao ◽

...

Keyword(s):

Genetic Diversity ◽

Genetic Variation ◽

Genetic Differentiation ◽

Genetic Relationships ◽

Inter Simple Sequence Repeat ◽

Phytophthora Sojae ◽

Anhui Province ◽

Population Variation ◽

Spatial Distance ◽

Similarity Coefficients

To explore genetic differentiation and the genetic relationships of Phytophthora sojae in Anhui Province, the inter-simple sequence repeat (ISSR) technique was used to analyze the genetic diversity of P. sojae. One hundred and sixty ISSR fragments were observed, including 129 (80.6%) polymorphic bands. This suggested that abundant genetic diversity existed among P. sojae in Anhui Province. The pairwise genetic similarity coefficients among the 62 strains ranged from 0.72 to 0.96, with a mean value of 0.85, indicating that there was a high level of genetic variation. Phytophthora sojae strains were divided into five clusters based on neighbor-joining (NJ) analysis, and the clustering was not related to geographic source, according to Mantel’s test (r = 0.3938). In addition, the clustering of strains from the same geographical source had little relationship to the year of collection. Analysis of molecular variance (AMOVA) showed that 16.65% of the genetic variation was derived from the collection area and 83.35% of the genetic variation was within-population variation. The genetic flow between different geographical sources ranged from 0.623 to 2.773, with a mean of 1.325, suggesting that gene exchange was frequent. Genetic distance and the genetic differentiation coefficient were not related to spatial distance.

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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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