Peering behind the curtain: how genetic context and fluctuating environments help to maintain alternative mating tactics

A blog post by Kathryn Stewart (@Kat_A_Stewart) on our paper “ The role of genetic diversity in the evolution and maintenance of environmentally-cued, male alternative reproductive tactics” by Stewart et al. (2019), published in BMC Evolutionary Biology. 19:58.

nature-nurture-1.jpgPhilosophers, psychologists, sociologists, and scientists have pitted nature vs. nurture against one another for a long time. In fact, one might be as so bold as to state it’s one of the oldest philosophical debates: a death-match if you will. In one corner, Nature, where genetics (or the unchangeable blueprints one is born with) remain the sole responsible party for all character traits. In the other corner, Nurture, in which the environment dictates who we are and how we act. While some academics, and truthfully some real-world examples, seem to be more one-sided than the other, for the most part experts now agree that both Nature and Nurture combine to play a pivotal role in how an organism looks and behaves.

Despite this, many steadfast researchers find it very difficult to track the contributions of both influences simultaneously, and this is never more present than when talking about traits that seem to readily change within an individual depending on the environmental circumstance. Phenotypic plasticity for example, is the ability for an organism to change how it responds to the environment regardless of its genetic composition; a classic example of Nurture, or so we once thought. Now, even phenotypically plastic traits (like height, aggression, growth curves, mating behavior, etc) are posited to have some associations to genetics that make them more or less predisposed to certain phenotypic trajectories (i.e. liability). But unpacking these contributions is often fraught with difficulty. If for example, genetics can contribute to traits that change based on altered environments, they likely aren’t major mutations and are thus difficult to trace. In fact, it would make sense that cryptic genetic variation (or the genetic context of an individual) actually underlies such multifaceted compositions of fitness.

OPowerPoint Presentationur new paper in BMC Evolutionary Biology looks to tackle this grey area between Nature and Nurture, using our model species, the bulb mite (Rhizoglyphus robini), where fighters possess weapons (thick muscular legs with sharp ends that can be used to kill conspecifics), whereas scramblers are defenceless. On one side, we have evidence to suggest bulb mite males adopt alternative reproductive tactics (ARTs) (fighters and scramblers) due to different developmental environments, and that this frequency of adoption sways back and forth depending on the current (and perceived future) state (see e.g. this blog post). On the other side, we have evidence of some heritability of these mating tactics (Smallegange & Coulson 2011), and transcriptomic expression profiles illustrate a markedly different pattern between male morphs (Joag et al. 2016), suggesting some genetic basis. Still, these Nature-Nurture attributes that affect adult phenotypes have remained isolated, placed in silos (or separate research programs in this case) making mating tactic evolution difficult to resolve for this species.

By looking at cryptic genetic diversity via never-before-published individual markers, our research team was able to show that these alternative male reproductive tactics actually comprise a genetic-by-environment interactions whereby both the environment and genotype of individuals influences their developmental (and thus mating) trajectory (see Figure 1 below).

bmc-post-figure.jpg

Figure 1. Genetic differentiation (FST) of male alternative reproductive tactics to the total population within each food environment (rich or poor food). Significant differences are represented above bars, * p < 0.05, ** p < 0.001. Images kindly supplied by F.T. Rhebergen.

Nature-Nurture interaction also helps to explain how this phenotypic and genetic variation is maintained within populations.  When environments are good, male morphs display different levels of inbreeding load such that fighters demonstrate high levels (and scramblers low levels) of homozygosity; in poor environments though, homozygosity decreases. Scrambler males and females also show similar levels of heterozygosity in poor environments, raising further questions of why we find such differential inbreeding (or lack thereof) costs. Does the fighter phenotype require a specific coordinated genetic architecture compared to scrambler males? Are inbred fighters less likely to be purged within populations during good environmental conditions compared to their counterparts or during stressful times, or alternatively, are the costs of inbreeding load higher for scramblers and females in general?

These and other questions will need to be fleshed-out a bit more in the future, but at least we are starting to bridge Nature-Nurture perspectives and hopefully disparate research programs in the bulb mite system. Importantly,  peering behind the curtain of phenotypes into individual genetic contexts will help to broaden our understanding of the complex interactions involved in life-history evolution.

References

Joag R, Stuglik M, Konczal M, Plesnar-Bielak A, Skrzynecka A, Babik W, et al. 2016. Transcriptomics of intralocus sexual conflict: gene expression patterns in females change in response to selection on a male secondary sexual trait in the bulb mite. Genome Biol Evol. 8:2351–7. ttps://doi.org/10.1093/gbe/evw169.

Smallegange IM, Coulson T. 2011. The stochastic demography of two coexisting male morphs. Ecology 92:755-764.

Stewart KA, Draaijer R, Kolasa MR, Smallegange IM. 2019. The role of genetic diversity in the evolution and maintenance of environmentally-cued, male alternative reproductive tactics.  BMC Evolutionary Biology. 19:58. DOI: 10.1186/s12862-019-1385-4

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