Lineage isolation in the face of active gene flow in the coastal plant wild radish is reinforced by differentiated vernalisation responses

Abstract

BackgroundThe respective role and relative importance of natural selection and gene flow in the process of population divergence has been a central theme in the speciation literature. A previous study presented conclusive evidence that wild radish on Japanese islands comprises two genetically isolated lineages: the southern and northern groups. However, a general understanding of the lineage isolation with frequent seed flow of the coastal plant species is still unclear. We surveyed nucleotide polymorphisms over 14 nuclear loci in 72 individuals across the Japan–Ryukyu Islands Arc to address the demographic history of wild radish utilising the isolation-with-migration (IM) model. In addition, we investigated the flowering times of individuals in different wild radish lineages, with and without cold exposure, to assess their respective vernalisation responses.ResultsCoalescent simulations suggested that divergence between the southern and northern lineages of wild radish began ~18,000 years ago, initially during the Last Glacial Maximum (LGM) period. The gene flow from the southern to northern groups was considerably higher than that in the opposite direction, indicating effective dispersal of viable seeds via the northward Kuroshio Current. Our greenhouse experiments indicated that cold exposure was not required for flowering in the southern group, but could advance the date of flowering, suggesting that vernalisation would be facultative in the southern group. In contrast, the northern group was either unable to flower or flowered later without prior cold exposure, and thus had an obligate requirement for cold treatment.ConclusionsThe south–north lineage divergence in wild radish could be triggered by a directional change in the sea current during the ice age, despite gene flow due to the high dispersability and longevity of seeds. We also found that temperature profoundly affected the vernalisation responses of wild radish, which may repress reproductive success and ultimately drive and reinforce intra-specific differentiation between the two lineages of wild radish. This study provides new insights into the maintenance of lineage differentiation with on-going gene flow in coastal plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0655-7) contains supplementary material, which is available to authorized users.

Interspecific Divergence of Two Sinalliaria (Brassicaceae) Species in Eastern China

“…However, we dated two species' divergence to within the Pleistocene (Figure 6 , Table 4 ) although such calculations should be treated cautiously because of the no-fossil calibrated mutation rate and the sequence variation from the limited loci. In addition, we detected extremely low gene flow between two species based on the sequence variations of nine nuclear loci, much lower than rates detected between other pairs of species that diverged recently, especially during the Pleistocene (Ikeda et al, 2009 , 2012 ; Wang et al, 2013 ; Han et al, 2016 ).…”

“…First, numerous ancient genera and species may have persisted due to geographical and ecological heterogeneity that could buffered the organisms from small-scale extinctions caused by the climate oscillations in eastern Asia, in conjunction with the lack of Pleistocene glaciation and subsequent large-scale extinctions. Second, many young species (for example, four Dysosma species, D. pleiantha, D. versipellis, D. difformis , and D. majoensis ) have originated through fast divergence probably driven by Pleistocene climate oscillations in conjunction with physiographic heterogeneity (Ikeda et al, 2012 ; Han et al, 2016 ; Wang et al, 2017 ). Both hypotheses have been partly tested based on biogeographic analyses of a few genera and phylogeographic examinations of some widely distributed species (see summaries by Qiu et al, 2011 ; Liu et al, 2012 ).…”

“…The direct evidence for such hypotheses should derive from the times and processes of the well-delimitated sister species that may have occurred during the Pleistocene (Zanella et al, 2016 ; Wang et al, 2017 ). Although Ikeda et al ( 2012 ), Han et al ( 2016 ), and Wang et al ( 2017 ) have revealed the Pleistocene origins of a pair of endemic alpine species, two coastal wild radish lineages and four understory herbs based on population genetic data, it remains unknown whether these species or lineages were morphologically differentiated with stable distinct characters and reproductively isolated as “good species” based on the integrate species concept (Liu, 2016 ).…”

Analyses of genome‐scale variation reveal divergence of two Sinalliaria species (Brassicaceae) with continuous but limited gene flow

“…Despite numerous caveats (e.g., the small number of individuals sampled from each species and likely ILS), these findings recover the complex species divergence process in eastern China during the Pleistocene. Our results therefore enrich our understanding of species diversity in eastern Asia and complement previously reported examples of Pleistocene plant speciation in this region (e.g., Martín‐Bravo et al, ; Ikeda et al, ; Levsen et al, ; Wang et al, ; Han et al, ).…”

“…The high species diversity of eastern Asia has been partly attributed to the absence of widespread plant extinction caused by the development of large glacial sheets, and partly to geographic isolations driven by Pleistocene climate oscillations that favored the evolution of young species (Tiffney, 1985;Axelrod et al, 1996;Qian & Ricklefs, 2004). This hypothesis was partly supported by phylogeographic and speciation studies of a few lineages occurring in eastern Asia (Qiu et al, 2011;Ikeda et al, 2012;Han et al, 2016). An inferred speciation history of sister species, the regional endemic Cardamine nipponica Franch.…”