A theoretical muddle of the conditional strategy: a comment on Neff and Svensson

Abstract

] recently reviewed the literature relating to the theoretical modelling of alternative mating tactics. Their review presents insightful future perspectives on how genomics could unveil the molecular genetics and proximate mechanisms of tactic expression, and we fully agree with their statements that a better understanding of the field can be achieved through the integration between quantitative and molecular genetics. However, we feel that it is important to draw attention to two significant oversights: their review (i) neglects previous studies that provided theoretical and empirical contributions to the understanding of the genetics underlying the conditional expression of alternative mating tactics (i.e. conditional strategies) and (ii) presents ideas that have been previously published (by other authors) as a new 'unified theory for the evolution and phenotypic expression of alternative mating tactics'. Below we elaborate why we believe that Neff and Svensson's verbal model ('the conditional alternative strategy') is not a new model, but is instead based on a misinformed view that current models do not account for genetic variation underlying conditional strategies. As a result, Neff and Svensson's 'conditional alternative strategy' unnecessarily muddles our understanding of conditional strategies.Phenotypic plasticity is a ubiquitous evolutionary phenomenon [2] and nowhere perhaps, is plasticity more apparent than when single genotypes can produce different alternative phenotypes depending upon environmental conditions [3]. Such polyphenisms are synonymous with conditional strategies and have been described in a wide range of traits, including the presence, shape and colour of morphological traits, alternative mating tactics, diet, sex and caste determination, as well as paedogenesis and diapause [4]. Understanding their genetic architecture and evolution is therefore vital for our understanding of these important adaptations. Dawkins' conditional evolutionary stable strategy model [5] provided an important theoretical framework for understanding polyphenisms, but also conveyed the message that genetic polymorphism is not necessary for a conditional strategy to be evolutionary stable. This message was an attempt to distinguish conditional strategies from 'alternative strategies', which represent a genetic polymorphism with Mendelian inheritance. However, it also led numerous authors to erroneously associate conditional strategies with complete genetic monomorphism [1,6,7]. It is well established, however, that underlying genetic variation is prevalent in plastic traits [8,9], and its role in polyphenisms has been modelled [10,11] and supported empirically numerous times [12 -15]. The conditional strategy was recently criticized based on this false assumption of genetic monomorphism [7]-a misconception that was subsequently laid to rest [16]. Neff and Svensson do cite this [16] correction of the record, but in our view failed to convey an understanding of its content, because the assumption of monomorphism ...

The role of genes and environment in the phenotypic expression of alternative mating tactics: a reply to Buzatto et al.

“…We see no utility in contrasting such statements to formal mathematical or quantitative genetic models for discrete polyphenisms as is advocated by Buzatto et al [1]. Those authors also seem to have a very restrictive use of the term model; one gets the impression that only formal mathematical models are counted as models.…”

“…Finally, we get the impression that Buzatto et al [1] equate genetics with quantitative genetics, which is a restricted view of the field of genetics. Genetics encompasses several subfields, including Mendelian, population and quantitative genetics, molecular genetics, genomics and transcriptomics.…”

“…We believe that a better understanding of the systems biology along with integration between classical quantitative genetic models and genomic information is necessary to understand the evolution of alternative mating tactics. Such a line of research that integrates molecular and classical quantitative genetics, as opposed to a more restricted quantitative genetic statistical approach advocated by Buzatto et al [1], is likely to lead to novel insights. A more integrative approach could, for instance, uncover the core 'decision' gene that underlies Gross's [7] status-dependent selection model for a conditional strategy.…”

“…

Buzatto et al [1] state that our recommendation to bring together previous, dichotomous game-theoretical approaches of modelling alternative strategies and a conditional strategy is unnecessary as fusion synthesis of this kind has already been carried out via the environmental threshold model. By presenting a verbal model in the conclusion and future direction section of our review paper, these authors state that we have developed a 'new theory' that is unnecessary.

As detailed in our review paper [2], we generally agree with the authors that there has been excellent past work on the quantitative genetics of polyphenisms, including in the area of alternative mating tactics.

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Investigating the genetic architecture of conditional strategies using the environmental threshold model

“…Owing to the predominance of environmental influence over genetic control, the genetic component is often overlooked when studying conditional strategies. However, genetic variation still plays a central role [12], because a 'pure polyphenism' or 'pure conditional strategy', with no genetic variance underlying the response to the environment, can only be manifested in clonal populations that lack genetic variation [13]. In fact, the role of genetic variation in polyphenisms [14][15][16] should be expected, because it allows adaptive evolution on ecological timescales in changing environments, keeping phenotypes close to their optimum [17].…”