Global biogeographic patterns in bipolar moss species

Abstract

A bipolar disjunction is an extreme, yet common, biogeographic pattern in non-vascular plants, yet its underlying mechanisms (vicariance or long-distance dispersal), origin and timing remain poorly understood. Here, combining a large-scale population dataset and multiple dating analyses, we examine the biogeography of four bipolar Polytrichales mosses, common to the Holarctic (temperate and polar Northern Hemisphere regions) and the Antarctic region (Antarctic, sub-Antarctic, southern South America) and other Southern Hemisphere (SH) regions. Our data reveal contrasting patterns, for three species were of Holarctic origin, with subsequent dispersal to the SH, while one, currently a particularly common species in the Holarctic (Polytrichum juniperinum), diversified in the Antarctic region and from here colonized both the Holarctic and other SH regions. Our findings suggest long-distance dispersal as the driver of bipolar disjunctions. We find such inter-hemispheric dispersals are rare, occurring on multi-million-year timescales. High-altitude tropical populations did not act as trans-equatorial 'stepping-stones', but rather were derived from later dispersal events. All arrivals to the Antarctic region occurred well before the Last Glacial Maximum and previous glaciations, suggesting that, despite the harsh climate during these past glacial maxima, plants have had a much longer presence in this southern region than previously thought.

Keywords: Polytrichaceae; Polytrichastrum; bipolar disjunction; bryophyte.

Figure 1.

Locations of ITS 1 + 2 (red) and ITS 2 only (orange) samples of P. juniperinum (a), P. strictum (b), P. piliferum (c) and P. alpinum (d). Known global distributions of the different species (shown in green) are reproduced from [5].

Figure 2.

Bayesian phylogenies constructed with (a) plastid marker trnL-F and (b) nuclear marker ITS (1 + 2) for P. alpinum, P. piliferum, P. strictum and P. juniperinum. PP and bootstrap support are shown next to branches (*conflict between topologies of Bayesian and ML tree; see electronic supplementary material, figures S1 and S2 for ML phylogenies). Colours refer to different geographical regions (see map); outgroups are indicated in black. The scale bar represents the mean number of nucleotide substitutions per site. ABGD species delimitation clusters with different p_max-values are shown in grey next to (b).

Figure 3.

Haplotype network of ITS 1 + 2 of (a) P. juniperinum, (b) P. strictum, (c) sister species P. juniperinum and P. strictum together, (d) P. piliferum and (e) P. alpinum. Separate haplotype networks of ITS 1 + 2 ((d,e) (i)) and ITS 2 only ((d,e)(ii)) are shown for the last two species. Haplotype circle sizes correspond to numbers of individuals with the same haplotype (see legend). Branches represent mutations between haplotypes, with mutations shown as one-step edges or as numbers. Colours refer to the different geographical regions (see map).

Figure 4.

Historical biogeography of four Antarctic Polytrichaceae mosses, highlighting the population history of P. juniperinum. The maximum clade credibility tree shows the median divergence time estimates calculated with two two-step dating analyses, with (a) or without (b) including the taxonomically uncertain fossil E. antiquum as a prior. Median ages and 95% height posterior distributions associated with major nodes are presented in electronic supplementary material, table S3. Coloured pie-charts represent ancestral range probabilities at each node as recovered by the best BioGeoBEARS model. Colours refer to the different geographical regions (see map). Arrows below the figure represent the time and direction of inter-hemispheric movements of all species excluding P. strictum. NH and SH represent Northern and Southern Hemispheres, respectively. The black line below each arrow is the branch, and therefore, timeframe over which the inter-hemispheric movement (according to ancestral range probabilities) was estimated to have occurred (note that 95% height posterior distribution of these branches is not presented here).