Department of Evolutionary and Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, PO Box 94240, 1090 GE, Amsterdam, The Netherlands.
Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Slawkowska 17 St., 31-016, Krakow, Poland.
BMC Evol Biol. 2019 Feb 18;19(1):58. doi: 10.1186/s12862-019-1385-4.
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.
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.
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.
替代性生殖策略（ARTs）是个体在种群中最大限度地提高生殖成功率的普遍策略。即使对于条件依赖性状，共识假设大多数 ARTs 都涉及遗传和环境相互作用（GEIs），但迄今为止，量化个体对环境线索做出反应而改变表型的遗传变异一直是一项艰巨的任务。我们的研究旨在调查环境差异明显的微小球茎螨（Rhizoglyphus robini）种群中 ART 的起源和维持，这些种群表现出“斗士”和“混战者”雄性形态，由复杂的环境和遗传因素组合介导。
使用从未发表过的个体遗传分析，我们发现除了应激环境中的混战者雄性外，所有个体在种群中都高度近交。事实上，在恶劣环境中，与其他所有比较相比，混战者雄性和雌性的遗传分化（Fst）没有显著差异，尽管在恶劣或良好环境中，斗士与其余种群高度分化（例如，Fst，STRUCTURE），但在恶劣环境中，斗士与种群的遗传分化程度约为其三倍。AMOVA 分析进一步证实了亚种群之间、形态和性别之间以及每个环境内亚种群之间的遗传分化。
我们的研究为球茎螨中的 ART 起源提供了新的见解，强调了遗传相互作用的重要性：遗传相关、上位相互作用以及环境胁迫下的性别特异性近交衰退。不对称的生殖产出，加上环境波动期间高度近交个体的清除，也促进了种群内的遗传变异，尽管存在强烈的定向选择证据。这种隐蔽的遗传变异也可以设想促进种群的稳定持续存在，即使面临空间或时间上不稳定的环境挑战。最终，了解维持阈值的遗传背景，即使是对于条件依赖的 ARTs，也将增强我们对种群内变异的理解，并提高我们预测对选择的反应的能力。
