Speciation in the presence of gene flow: population genomics of closely related and diverging Eucalyptus species

Abstract

Speciation is a complex process that is fundamental to the origins of biological diversity. While there has been considerable progress in our understanding of speciation, there are still many unanswered questions, especially regarding barriers to gene flow in diverging populations. Eucalyptus is an appropriate system for investigating speciation mechanisms since it comprises species that are rapidly evolving across heterogeneous environments. We examined patterns of genetic variation within and among six closely related Eucalyptus species in subgenus Eucalyptus section Eucalyptus in south-eastern Australia (commonly known as the "green ashes"). We used reduced representation genome sequencing to genotype samples from populations across altitudinal and latitudinal gradients. We found one species, Eucalyptus cunninghamii, to be highly genetically differentiated from the others, and a population of mallees from Mount Banks to be genetically distinct and therefore likely to be a new undescribed species. Only modest levels of differentiation were found between all other species in the study. There was population structure within some species (e.g., E. obstans) corresponding to geographical factors, indicating that vicariance may have played a role in the evolution of the group. Overall, we found that lineages within the green ashes are differentiated to varying extents, from strongly diverged to much earlier stages of the speciation continuum. Furthermore, our results suggest the green ashes represent a group where a range of mechanisms (e.g., reticulate evolution and vicariance) have been operating in concert. These findings not only offer insights into recent speciation mechanisms in Eucalyptus, but also other species complexes.

Landscape drivers of genomic diversity and divergence in woodland Eucalyptus

“…About half of all common variants discovered in this study are common in both species, and we observed low genome‐wide divergence between E. albens and E. sideroxylon ( F ST = 0.15). Recent evidence suggests the genetic divergence is not strong at most genomic loci in many species, both in eucalypts (Rutherford et al, ) and more broadly (Andrew & Rieseberg, ; Wu, ). Additionally, low interspecific differentiation is expected theoretically given extremely large effective population sizes, long generation times and relatively recent radiation (González‐Orozco et al, ).…”

Restore and Renew: a genomics‐era framework for species provenance delimitation

“…Reduced representation sequencing approaches, such as DArTseq, enable the cost‐effective investigation of evolutionary processes at a genomic scale and the fine‐scale examination of genetic variation across landscapes (Bragg et al ). Recent studies using DArTseq have found that they are informative for understanding relationships among populations and species, particularly in closely related lineages (Yang et al ; Melville et al ; Rutherford et al ).…”

Landscape drivers of genomic diversity and divergence in woodland Eucalyptus

“…About half of all common variants discovered in this study are common in both species, and we observed low genome-wide divergence between E. albens and E. sideroxylon (F ST = 0.15). Recent evidence suggests the genetic divergence is not strong at most genomic loci in many species, both in eucalypts (Rutherford et al, 2018) and more broadly (Andrew and Rieseberg, 2013;Wu, 2001). Additionally, low interspecific differentiation is expected theoretically given extremely large effective population sizes, long generation times, and relatively recent radiation (González-Orozco et al, 2016).…”

“…The prevalence of discrete population structure, IBD and/or IBE has been studied in several eucalypt species (e.g. Andrew et al, 2005Andrew et al, , 2007Jones et al, 2007;Jordan et al, 2017;Rutherford et al, 2018;Steane et al, 2006Steane et al, , 2015Steane et al, , 2014Supple et al, 2018). Although eucalypts have very limited seed dispersal, they generally preferentially outcross and are pollinated by generalist bird and insect pollinators, both of which contribute to their spatial genetic structure (Booth, 2017;Potts and Gore, 1995;Williams and Woinarski, 1997).…”