Reinventing the wheel? Reassessing the roles of gene flow, sorting and convergence in repeated evolution

Abstract

Biologists have long been intrigued by apparently predictable and repetitive evolutionary trajectories inferred across a variety of lineages and systems. In recent years, high‐throughput sequencing analyses have started to transform our understanding of such repetitive shifts. While researchers have traditionally categorized such shifts as either “convergent” or “parallel,” based on relatedness of the lineages involved, emerging genomic insights provide an opportunity to better describe the actual evolutionary mechanisms at play. A synthesis of recent genomic analyses confirms that convergence is the predominant driver of repetitive evolution among species, whereas repeated sorting of standing variation is the major driver of repeated shifts within species. However, emerging data reveal numerous notable exceptions to these expectations, with recent examples of de novo mutations underpinning convergent shifts among even very closely related lineages, while repetitive sorting processes have occurred among even deeply divergent taxa, sometimes via introgression. A number of very recent analyses have found evidence for both processes occurring on different scales within taxa. We suggest that the relative importance of convergent versus sorting processes depends on the interplay between gene flow among populations, and phylogenetic relatedness of the lineages involved.

Genetic basis of speciation and adaptation: from loci to causative mutations

“…Identification of causative mutations also contributes to a better understanding of the repeatability of evolution [ 7 , 42 ]. Genetic studies of convergent evolution have revealed hotspot genes that are repeatedly used for getting the same phenotypes [ 20 , 43 – 45 ]. In several cases, the same mutation repeatedly occurs at the same site in independent lineages [ 20 , 46 , 47 ].…”

Editorial 2022

“…With the rapid development of next‐generation sequencing, it is now possible to access the genetic mechanisms behind this convergence. Waters and McCulloch (2021) wrote a synthesis of recent genomic analyses confirming that convergence is the predominant driver of replicated evolution among species, whereas repeated sorting of standing variation is the major driver of repeated shifts within species. Numerous notable exceptions to these expectations exist, with for example de novo mutations underpinning convergent shifts among very closely related lineages, and replicated sorting processes occurring among even deeply divergent taxa, sometimes via introgression. The number of environmental DNA (eDNA) studies of freshwater environments has increased dramatically in recent years.…”

Contribution of hybridization to the evolution of a derived reproductive strategy in ricefishes

“…Alternatively, the evolution of similar phenotypic traits in different species can also be due to introgression or repeated sorting of shared standing genetic variation. Introgressed variation from one into another population or even species may facilitate the implementation of adaptive variants which are identical by descent (Waters & McCulloch 2021). This so-called adaptive introgression provides fast access to additional genetic variation, if species boundaries are weak (Mallet 2005; Whitney et al 2006; Arnold 2007; Baack & Rieseberg 2007; Castric et al 2008; Rieseberg 2009; The Heliconius Genome Consortium et al 2012; Seehausen 2004).…”

“…It was proposed that a high level of introgression led to the rapid radiation of Heliconius butterflies (Edelman et al 2019), similar to Darwin’s finches (Lamichhaney et al 2015) and African Cichlids (Meier et al 2017). Convergent evolution by repeated sorting (Waters & McCulloch 2021) involves alleles identical by descent, regardless of the potential source of variation, which may be recent (Colosimo et al 2005; Terekhanova et al 2014) or rather ancient (Nelson & Cresko 2018; Van Belleghem et al 2018; van der Valk et al 2021; Veale & Russello 2017; Brawand et al 2014).…”