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

Abstract

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. Electronic supplementary material The online version of this article (10.1186/s12862-019-1385-4) contains supplementary material, which is available to authorized users.

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

“…Additional food and water were provided to each stock container once or twice per week (in a manner similar to [44]). The observed heterozygosity (averaged across sex and ART) of the stock populations was measured at 0.39 for the rich environment and 0.48 for the poor environment (50).…”

“…Upon maturity, male R. robini develop into one of two distinct morphs (see Figure 1): (1) juvenile males that are relatively large mostly mature as "fighters", which possess a thickened third leg pair with a sharp end that can be used to kill conspecifics [45,46], and (2) juvenile males that are relatively small mostly mature as "scramblers", which lack the weaponized leg pair (although a rare third morph, the megascrambler, has recently been suggested; [47]). Although scrambler expression is regulated by a (partially) genetically determined threshold for body size [17; 48; 49], gene-by-environment interactions also play a key role [50], with diet quality and quantity thought to be the primary drivers of body size and therefore ART expression [18]. Despite this, the selection pressures that maintain the coexistence of fighters and scramblers are still not fully understood.…”

“…Despite this, the selection pressures that maintain the coexistence of fighters and scramblers are still not fully understood. Numerous studies have attempted to identify or quantify the fitness functions that underlie this evolutionary maintenance [17,42,44,48,[50][51][52], but some facets of bulb mite ecology, such as its chemical communication, remain unexplored in this context.…”

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

“…1 A): (1) juvenile males that are relatively large mostly mature as “fighters”, which possess a thickened third leg pair with a sharp end that can be used to kill conspecifics [ 44 , 45 ], and (2) juvenile males that are relatively small mostly mature as “scramblers”, which lack the weaponized leg pair (although a rare third morph, the mega-scrambler, has recently been suggested; [ 46 ]). Although scrambler expression is regulated by a (partially) genetically determined threshold for body size [ 17 , 47 , 48 ] with varying degrees of heritability [ 47 , 49 ], gene-by-environment interactions also play a key role [ 50 ], with temperature [ 51 ], and importantly diet quality and quantity thought to be the primary drivers of body size and therefore ART expression [ 18 ]. Despite this, the selection pressures that maintain the coexistence of fighters and scramblers are still not fully understood.…”

“…Despite this, the selection pressures that maintain the coexistence of fighters and scramblers are still not fully understood. Numerous studies have attempted to identify or quantify the fitness functions that underlie this evolutionary maintenance [ 17 , 41 , 43 , 47 , 50 , 52 , 53 ], but some facets of bulb mite ecology, such as its chemical communication, remain unexplored in this context.

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