A simple conceptual framework and nomenclature for studying repeated, parallel and convergent evolution

Abstract

Parallel and convergent evolution are textbook examples of the role of natural selection in evolution. However, these terms are used interchangeably, and sometimes with conflicting meanings. This has resulted in confusion, which hampers the understanding of the processes underlying these important forms of evolution. In this synthesis, I discuss the issues with current definitions of parallel, repeated and convergent evolution, and provide a framework aimed at solving these issues. This framework makes an important distinction between environmental properties and organismal properties, with the first involving the role of similar and non-similar environmental and selective pressures. The organismal properties include the genomic-basis where the process (mutation, standing genetic variation and gene flow) and the location (homologous nucleotide, homologous gene region or non-homologous gene region) are emphasised, and the phenotype (convergent or parallel evolved). I restrict the use of the terms parallel (evolution of similar and derived phenotypes, from similar ancestral phenotypes) and convergent (evolution of similar and derived phenotypes, from dissimilar ancestral phenotypes) evolution to the phenotypic level, thereby restoring its original meaning before the genomic revolution. I argue that this framework and nomenclature provide a clear resolution to study parallel and convergent phenotypic evolution across fields while maintaining the interest in its genomic and ecological grounds. Crucially, this framework stresses the importance of a multidisciplinary focus, integrating ecology, genomics, and phenotypes to determine whether parallel or convergent phenotypic evolution has taken place.

Multiple paths towards repeated phenotypic evolution in the spiny-leg adaptive radiation (Tetragnatha; Hawaii)

“…The copyright holder for this preprint this version posted December 2, 2022. ; https://doi.org/10. 1101/2022 to output all sequencing positions, even those with 0 depth; Supplementary Table 01). We then processed the data using ANGSD v0.935 (Kousathanas et al 2017), a pipeline designed to handle and analyze low coverage sequencing data.…”

“…The copyright holder for this preprint this version posted December 2, 2022. ; https://doi.org/10. 1101/2022 The Hawaiian Tetragnatha spiny-leg species belong to a clade comprising ~17 species, and are part of a large radiation endemic to the archipelago (Gillespie 2016;Kennedy et al 2022). These species can be grouped into four ecomorphs (Figure 1 A-D), which are linked to the substrate they inhabit (Gillespie 2004): the Large Brown ecomorph is found on tree bark (Figure 1A), the Green ecomorph on leaves (Figure 1B), the Maroon ecomorph on mosses (Figure 1C), and the Small Brown ecomorph on twigs (Figure 1D).…”

“…Of particular interest in adaptive radiation is the repeated phenotypic evolution (i.e. parallel or convergent phenotypic evolution) (Cerca 2022), where equivalent phenotypes evolve in response to similar ecological challenges (Losos and Ricklefs 2009; Losos 2010). Repeated evolution of similar phenotypes has been found in multiple radiations and offers a powerful approach for disentangling recurrent and potentially-deterministic phenotypic outcomes in response to similar environmental conditions (Losos 2010, 2011; Gillespie et al 2018, 2020; Malinsky et al 2018; Salzburger 2018; Masonick et al 2022; Urban et al 2022).…”

Multiple paths toward repeated phenotypic evolution in the spiny‐leg adaptive radiation (Tetragnatha; Hawai'i)

“…The repeated evolution of phenotypes, commonly referred to as parallel or convergent evolution (Cerca, 2022;James et al, 2023), is a particularly fascinating aspect of adaptive radiations as it provides valuable insights into the extent to which phenotypic outcomes in response to similar environmental conditions are predictable (Gillespie et al, 2018(Gillespie et al, , 2020Losos, 2010Losos, , 2011Losos & Ricklefs, 2009;Malinsky et al, 2018;Masonick et al, 2022;Salzburger, 2018;Urban et al, 2022). For example, the repeated evolution of habitat specialists has been documented in multiple adaptive radiations including the Caribbean Anolis lizards (Losos & Ricklefs, 2009), Hawaiian Tetragnatha (Gillespie, 2004), cichlid fishes (Sowersby et al, 2021) and Ariamnes spiders (Gillespie et al, 2018).…”

“…The repeated evolution of phenotypes or ecomorphs can result from three evolutionary processes that are not mutually exclusive and that can occur at different regions of the genome (Cerca, 2022; Lee & Coop, 2017, 2019; Pease et al, 2016; Stern, 2013): mutation (either de novo or larger mutational events, where different mutations cause similar phenotypes), shared ancestral polymorphism (standing variation, where old genetic variation is recruited) or gene flow (where an allele is recruited from one lineage to another). These three patterns have been observed in the context of adaptive radiations (Choi et al, 2021; De‐Kayne et al, 2022; Meier et al, 2018; Richards & Martin, 2017; Salzburger, 2018; Sowersby et al, 2021) and, because they leave distinct footprints along the genome, the use of genomic‐level data makes it possible to distinguish the contribution of each of these processes (Barrett & Schluter, 2008; Lee & Coop, 2017, 2019).…”