Molecular ecology studies of species radiations: current research gaps, opportunities and challenges

Abstract

Understanding the drivers and limits of species radiations is a crucial goal of evolutionary genetics and molecular ecology, yet research on this topic has been hampered by the notorious difficulty of connecting micro-and macroevolutionary approaches to studying the drivers of diversification. To chart the current research gaps, opportunities and challenges of molecular ecology approaches to studying radiations, we examine the literature in the journal MOLECULAR ECOLOGY and revisit recent high-profile examples of evolutionary genomic research on radiations. We find that available studies of radiations are highly unevenly distributed among taxa, with many ecologically important and species-rich organismal groups remaining severely understudied, including arthropods, plants and fungi. Most studies employed molecular methods suitable over either short or long evolutionary time scales, such as microsatellites or restriction site-associated DNA sequencing (RAD-seq) in the former case and conventional amplicon sequencing of organellar DNA in the latter. The potential of molecular ecology studies to address and resolve patterns and processes around the species level in radiating groups of taxa is currently limited primarily by sample size and a dearth of information on radiating nuclear genomes as opposed to organellar ones. Based on our literature survey and personal experience, we suggest possible ways forward in the coming years. We touch on the potential and current limitations of whole-genome sequencing (WGS) in studies of radiations. We suggest that WGS and targeted ('capture') resequencing emerge as the methods of choice for scaling up the sampling of populations, species and genomes, including currently understudied organismal groups and the genes or regulatory elements expected to matter most to species radiations.

Recent secondary contacts, background selection and variable recombination rates shape genomic diversity in the model speciesAnolis carolinensis

“…However, studying the genetic bases of adaptation in anoles cannot be properly addressed without quantifying the patterns that can blur signatures of local adaptation, such as heterogeneous introgression (Roux et al 2014) or background selection (Hoban et al 2016). Moreover, the study of intraspecific genetic variation holds promise to address questions at larger evolutionary scale, such as the role of demography, selection and incompatibilities in the process of speciation and genome divergence (Figuet et al 2014; Romiguier et al 2014; Seehausen et al 2014; Chalopin et al 2015; de la Harpe et al 2017). Here we sequenced 27 genomes of green anoles and highlighted how secondary contact, expansions, but also heterogeneous recombination and purifying selection have shaped the genomic landscape of differentiation.…”

“…Thorough analyses of the factors affecting genome diversity at the peri-specific level have been performed in a small number of vertebrate species (see Ellegren et al , 2012; Sousa et al , 2013; Poelstra et al , 2014; Booker et al , 2017; Han et al , 2017; Kawakami et al , 2017) but several major clades of vertebrates have not been investigated at all. This need for higher resolution in genomic studies has been recently highlighted with several comments urging to “scale-up” the sequencing effort in studies of evolutionary radiations around the species level (Ellegren 2014; de la Harpe et al 2017). Among those are the non-avian reptiles, a speciose group of vertebrates that harbor a wide diversity of morphology and adaptation.…”

Phylogeography of the highly dispersible landscape‐dominant woody species complex,Metrosideros, in Hawaii

“…We analyze variation at nine nuclear microsatellite loci across 1,486 adults of nearly all known taxa and morphotypes sampled from five main Hawaiian Islands, plus additional populations from Tahiti and American Samoa. We combine a population genetics approach and broad taxonomic sampling (de la Harpe et al, 2017) to examine relationships across the island chain because the continuous distribution and woody habit of Metrosideros, along with frequent hybridization among its many closely related taxa, make phylogenetic approaches difficult. The following questions were addressed: Q1) How does genetic diversity vary across islands?…”

Lessons from a natural experiment: Allopatric morphological divergence and sympatric diversification in the Midas cichlid species complex are largely influenced by ecology in a deterministic way

“…Thus, studies of young radiations allow for insights into the immediate factors that drive diversification and can complement large‐scale macroevolutionary studies in important ways (de la Harpe et al. ; Recknagel et al. ).…”