Vicariance versus dispersal across Beringian land bridges to explain circumpolar distribution: A case study in plants with high dispersal potential

Abstract

Aim To disentangle the importance of the Beringian land bridges during the Pliocene and Quaternary periods in order to explain the current distribution of circumpolar plants with potential for long‐distance dispersal. Location Circumpolar (Arctic and Antarctic). Methods We sampled all extant species in Carex section Glareosae (26 species and 2 subspecies) and analysed 14 DNA regions, including the nrDNA regions ETS and ITS, three nuclear single‐copy genes (CATP, G3PDH and GZF), and nine cpDNA regions: 5′trnK intron, atpIH, matK, ndhJ‐trnF, psbA‐trnH, rpl32‐trnL, rps16, trnC‐ycf6 and ycf6‐psbM. After testing for outlier proportions, we used Bayesian inference, maximum likelihood and a species‐tree approach to infer phylogenetic relationships between species; divergence times were estimated using Beast2. We then performed biogeographical analyses using “BioGeoBEARS” to estimate ancestral areas by means of reticulate models. Finally, lineage through time (LTT) and diversification pattern analyses were performed using Bamm. Results Carex section Glareosae is a monophyletic group that diverged c. 6.56 Ma (4.54–8.51 Ma at 95% highest posterior density interval). We show that within‐area cladogenetic speciation events and anagenetic dispersal (including some vicariance events) play an important role in shaping distribution in species with potential for long‐distance dispersal. Diversification patterns show constant diversification rates over time. Main conclusions The Bering Strait may have played an important role in shaping the current distribution of the species in the section, facilitating dispersal between Asia and North America during glacial periods when the Beringian land bridges were open. Nevertheless, we cannot discount long‐distance dispersal as an alternative major force shaping the species distribution in the section.

A tale of worldwide success: Behind the scenes of Carex (Cyperaceae) biogeography and diversification

“…While this may just be ascertainment bias—the probability of detecting any significant clade‐level effects increases in larger clades, and subg. Carex and Vignea are by far the largest—it may also suggest a dispersal and colonization ability unique to these groups, as discussed in previous studies (Escudero et al, ; Jiménez‐Mejías et al, 2012b; Villaverde et al, , ; Maguilla et al, ). However, none of these groups identified as geographically widespread display clear anemochorous or epizoochorous traits (though the bent utricle beaks in some sect.…”

“…The inferred timing of biogeographic events (Fig. S5) strongly suggests that multiple, recurrent LDD events better explain Carex biogeographic patterns than tectonic vicariance or Northern Hemisphere land‐bridge hypotheses, perhaps with the exception of some relatively recent Beringian lineages (see Maguilla et al, ). The occurrence of dispersal events is clearly biased towards more recent times, especially to the last 10 My corresponding to the most recent 25% of the age of the genus.…”

“…Bipolar distributions at the species level have also been particularly well‐documented in Carex and explained mostly by direct long‐distance dispersal from the Northern Hemisphere to high latitudes of the Southern Hemisphere in South America and New Zealand (Villaverde et al, 2015a, 2015b, 2017b, 2017c; Márquez‐Corro et al, ; Maguilla et al, ). The genus also exhibits circumpolar (Gebauer et al, ; Hoffmann et al, ; Maguilla et al, ), Beringian (Schönswetter et al, ; King & Roalson, ; Maguilla et al, ), amphi‐Atlantic (Schönswetter et al, ; Jiménez‐Mejías et al, 2012b; Westergaard et al, ), Arctic‐Alpine (Schönswetter et al, , ; Jiménez‐Mejías et al, 2012a; Gebauer et al, ; Hoffmann et al, ), pan‐Himalayan (Uzma et al, ), Europe‐Central Asia (Schönswetter et al, ), East‐West Europe/Mediterranean (Escudero et al, , ; Jiménez‐Mejías et al, , 2012a; Míguez et al, ; Benítez‐Benítez et al, , ), and Eastern‐Western North America (Roalson & Friar, 2004a, 2004b; Hipp et al, ; Hipp, ; Dragon & Barrington, ) distribution patterns, all illuminated using phylogenetic approaches. Colonization of isolated oceanic archipelagos from mainland sources has also been documented by several authors; these include Hawaii (Dragon & Barrington, ), Macaronesia (Escudero et al, ; Jiménez‐Mejías et al, 2012b; Míguez et al, ), Mascarenes and Tristan da Cunha (Escudero et al, ), and Juan Fernández (Ridley & Jiménez‐Mejías, in prep.).…”

A pre‐Miocene Irano‐Turanian cradle: Origin and diversification of the species‐rich monocot genus Gagea (Liliaceae)

“…Therefore, it cannot be ruled out that G. serotina arrived to Northern America through long‐distance dispersal, without involving land bridges. This was also discussed, for example, for Carex section Glareosae (Maguilla et al, ).…”

“…At the Pliocene/Pleistocene boundary, the vegetation type of Beringia mostly comprised boreal forest‐tundra (Graham, ), so that migration from Asia was possible for cold‐tolerant species (Edwards, Lloyd, & Armbruster, ) such as G. serotina (Peruzzi, Tison, et al, ). The role of Beringia for the colonization of North America was discussed for several plant groups (tribe Lilieae: Huang et al, ; main Arabis clade of tribe Arabideae of the Brassicaceae: Karl & Koch, ; for further examples see Graham, ; Maguilla, Escudero, & Luceño, ). The flat seeds of Gagea serotina are adapted to dispersal by wind.…”