Genes versus phenotypes in the study of speciation

Abstract

Despite persistent debate on the nature of species, the widespread adoption of Mayr's biological species concept has led to a heavy emphasis on the importance of reproductive isolation to the speciation process. Equating the origin of species with the evolution of reproductive isolation has become common practice in the study of speciation, coincident with an increasing focus on elucidating the specific genetic changes (i.e.-speciation genes) underlying intrinsic reproductive barriers between species. In contrast, some have recognized that reproductive isolation is usually a signature effect rather than a primary cause of speciation. Here we describe a research paradigm that shifts emphasis from effects to causes in order to resolve this apparent contradiction and galvanize the study of speciation. We identify major elements necessary for a balanced and comprehensive investigation of the origin of species and place the study of so-called "speciation genes" into its appropriate context. We emphasize the importance of characterizing diverging phenotypes, identifying relevant evolutionary forces acting on those phenotypes and their role in the causal origins of reduced gene flow between incipient species, and the nature of the genetic and phenotypic boundaries that results from such processes. This approach has the potential to unify the field of speciation research, by allowing us to make better "historical" predictions about the fate of diverging populations regardless of taxon.

A recombination suppressor contributes to ecological speciation in OSTRINIA moths

“…The putative sex-linked inversion we document in Ostrinia appears consistent with the large-effect, multicomponent prediction of chromosomal rearrangement models of speciation. First, multiple 'speciation phenotypes' (Shaw and Mullen, 2011) in ECB have known sex-linked factors, including male pheromone response and diapause timing (McLeod, 1978;Dopman et al, 2004;Wanner et al, 2010;Ikten et al, 2011). Second, a recent study indicated that large isolation effect sizes are common between ECB strains (RI ⩾ 0.5 for 4 of 7 forms of isolation; Dopman et al, 2010).…”

Limnephilid taxa revised by speciation traits: Rhadicoleptus, Isogamus, Melampophylax genera, Chaetopteryx rugulosa, Psilopteryx psorosa species groups, Drusus bolivari, Annitella kosciuszkii species complexes (Trichoptera: Limnephilidae)

“…There is a debate whether inability to interbreed is only an integrated signature effect, the by-product of selection, that is the accumulated loss of reproductive compatibility, or it is the primary cause of speciation, the creator, the mechanism of selection. Phenotypic divergences between incipient species suggest causal interactions between divergent trait and gene flow restrictions during speciation (Shaw & Mullen 2011). Evolution works by screening phenotypes rather than genotypes.…”

“…Which diverging phenotypes involved, redundant or neutral in suppressing gene flow? Speciation phenotypes are those traits whose divergence contributes to a reduction of gene flow (Shaw & Mullen 2011). Phenotypic divergence, as a proximate instrument of speciation in sympatry or allopatry or via founder effect or reinforcement, rarely studied systematically.…”

“…Or could the reproductive isolation be a direct target of selection? Selectionist feel that emphasis on reproductive isolation obstructs the study of speciation as a product of divergent selection and shift the primary emphasis to environmental adaptation through natural selection (Shaw & Mullen, 2011). There is emphasis (Bonduriansky 2011) that sexual selection, as an engine of ecological diversification, could carry populations through fitness valleys of maladaptive intermediate phenotypes between alternative niches on the fitness landscape.…”

Fine phenomics applied to the Nectopsyche genus (Trichoptera) Species delineation by speciation traits

“…Speciation phenotypes are those traits whose divergence contributes to a reduction of gene flow (Shaw & Mullen 2011). Speciation traits are expressed phenotypes of speciation genes.…”