Pleistocene dynamics of the Eurasian steppe as a driving force of evolution: Phylogenetic history of the genus Capsella (Brassicaceae).

Anže Žerdoner Čalasan,Anna Seidl,Herbert Hurka,Frank R Blattner,Dmitry A German,Simon Pfanzelt,Barbara Neuffer

doi:10.1002/ece3.8015

Abstract

Capsella is a model plant genus of the Brassicaceae closely related to Arabidopsis. To disentangle its biogeographical history and intrageneric phylogenetic relationships, 282 individuals of all five currently recognized Capsella species were genotyped using a restriction digest‐based next‐generation sequencing method. Our analysis retrieved two main lineages within Capsella that split c. one million years ago, with western C. grandiflora and C. rubella forming a sister lineage to the eastern lineage consisting of C. orientalis. The split was attributed to continuous latitudinal displacements of the Eurasian steppe belt to the south during Early Pleistocene glacial cycles. During the interglacial cycles of the Late Pleistocene, hybridization of the two lineages took place in the southwestern East European Plain, leading to the allotetraploid C. bursa‐pastoris. Extant genetic variation within C. orientalis postdated any extensive glacial events. Ecological niche modeling showed that suitable habitat for C. orientalis existed during the Last Glacial Maximum around the north coast of the Black Sea and in southern Kazakhstan. Such a scenario is also supported by population genomic data that uncovered the highest genetic diversity in the south Kazakhstan cluster, suggesting that C. orientalis originated in continental Asia and migrated north‐ and possibly eastwards after the last ice age. Post‐glacial hybridization events between C. bursa‐pastoris and C. grandiflora/rubella in the southwestern East European Plain and the Mediterranean gave rise to C. thracica. Introgression of C. grandiflora/rubella into C. bursa‐pastoris resulted in a new Mediterranean cluster within the already existing Eurasian C. bursa‐pastoris cluster. This study shows that the continuous displacement and disruption of the Eurasian steppe belt during the Pleistocene was the driving force in the evolution of Capsella.

Highlights

Capsella Medik. is a small genus within the mustard family (Brassicaceae)
Such a scenario is supported by population genomic data that uncovered the highest genetic diversity in the south Kazakhstan cluster, suggesting that C. orientalis originated in continental Asia and migrated north-and possibly eastwards after the last ice age
This study shows that the continuous displacement and disruption of the Eurasian steppe belt during the Pleistocene was the driving force in the evolution of Capsella

Summary

| INTRODUCTION

Capsella Medik. is a small genus within the mustard family (Brassicaceae). Of all wild relatives of the model system Arabidopsis (DC.) Heynh., Capsella is the most closely related and intensively investigated genus. By including the commonly neglected species C. orientalis and C. thracica in molecular phylogenetic analyses, Hurka et al (2012) discovered the “missing link” in the understanding of the origin of tetraploid C. bursa-pastoris and provided evidence that in Capsella the transition from outbreeding to selfing at the diploid level occurred twice independently. This was later confirmed by several other studies, for example, Douglas et al (2015), Bachmann et al (2019), and Žerdoner Čalasan et al (2019). While Altai has been commonly recognized as a refugial area for steppe flora and fauna, we wanted to assess via ecological niche modeling whether this mountain range had the same refugial role in case of younger taxa, such as C. orientalis

| MATERIALS AND METHODS

Findings

| DISCUSSION