The Quaternary biogeographic history of bryophytes: a window into their ability to face global change

Studying the influence of past climate changes on the distribution of species contributes to our understanding of the evolution of life on earth. Among past climate changes, the Quaternary period (from 2.4 Myrs to present time), characterized by high amplitude climatic oscillations, is considered one main determinant of current species distributions. Europe has long served as a model region to study the impact of past climate changes on extant biodiversity patterns. Its landscape is characterized by the presence of E-W-oriented mountain ranges, acting as effective barriers to migration for many organisms. Explicit historical scenarios for the post-glacial recolonization of Europe from distinct refugia have been discussed at length in the literature. In contrast, the impact of past climate changes on species distributions in tropical areas has been much less documented. In Amazonia, where the landscape is homogeneous without any apparent geographic barrier to migration, available fossil evidence describes range contractions and expansions of the evergreen rainforest during the Quaternary period.
Bryophytes are poïkilohydric and therefore appear as extremely sensitive to climate changes. Bryophytes disperse by means of spores or asexual diaspores, which are involved in frequent long-distance dispersal (LDD) events. These high dispersal capacities have cast doubts on the possibility to find signatures of historical events from analyses of the extant spatial patterns of genetic structure and diversity of their populations. In Amazonia in particular, recent ecological work suggests that dispersal does not show geographical structure across the area.
In the present thesis, we assembled and analyzed large molecular datasets at the level of the species range to determine how bryophytes responded to major Quaternary climate changes in environments characterized by different ‘resistance’ to migration and environmental heterogeneity, especially in Europe and Amazonia (ongoing study in the case of the latter). More specifically, the aims are to: (1) Test whether, due to the high dispersal capacities of bryophytes in general – and in particular in homogeneous environments without any apparent geographic barrier to migration –, the inverse isolation hypothesis – according to which any signal of isolation-by-distance (IBD) is erased beyond the limits of short-distance dispersal (SDD) by the intensity of LDD events – applies, erasing any historical signal in the extant spatial patterns of genetic structure and diversity of bryophyte populations; (2) Test the relevance of other differentiation mechanisms promoting speciation and, in particular isolation-by-environment (IBE), across a relatively homogeneous environment without any apparent geographic barrier to migration; (3) Infer the post-glacial history of bryophytes, in environments characterized by the presence (Europe) or the absence (Amazonia, ongoing study) of apparent geographic barriers to migration, from analyses of the extant spatial patterns of genetic structure and diversity of their populations.
The results strongly suggest that the LDD capacities of bryophytes did not homogenize the genetic structure of their populations, neither in an environment characterized by apparent geographic barriers to migration – such as the E-W-oriented mountain ranges in Europe –, nor in a much more homogeneous environment as in the Amazonian rainforest. In contradiction with the idea that the inverse isolation hypothesis applies in Amazonian bryophytes in particular, the IBD signal observed in 8 out of the 10 Amazonian bryophyte species consistently remained significant beyond the range of SDD, evidencing LDD limitations. This consistent persistence of the IBD signal contrasts with the result of a recent meta-analysis on IBD patterns in bryophytes and suggests that Amazonian bryophyte species experience more dispersal limitations than species from other biomes. As a comparison, we showed that, within the same Amazonian environment, the spatial genetic structures observed in bryophytes are comparable to that of angiosperm species producing much larger seeds.
While a significant IBD signal characterizes the genetic structure of the vast majority of the Amazonian bryophyte species investigated here, our results are not consistent with the idea that isolation-by-resistance (IBR) and IBE contributed to the observed spatial patterns of genetic variation. Nevertheless, a low (0.059) but significant (P=0.004) Fst was found between sympatric specimens of the sibling Syrrhopodon annotinus and S. simmondsii, and their average kinship coefficients along a geographic gradient were consistently higher for conspecific comparisons than for interspecific comparisons, pointing to reproductive isolation between those two sympatric species characterized by different habitat requirements. Even if this single empirical result does not challenge the global idea that IBE does not prevail in extant patterns of genetic diversification in Amazonian bryophytes, it nonetheless contributes to growing evidence for genetic divergence observed along environmental gradients, suggesting that adaptation could play a more important role in shaping genetic patterns than previously thought.
Rejection of the hypothesis that high dispersal capacities of bryophytes erased any historical signal in the extant spatial patterns of genetic structure and diversity of their populations and, in particular rejection of the inverse isolation hypothesis, indicate that the data generated in the present thesis are suitable for demographic inference. We applied coalescence-based approaches to infer the post-glacial history of bryophyte populations from contrasting environments characterized by the presence (Europe) or the absence (Amazonia, ongoing study) of apparent geographic barriers to migration. In Europe, our analyses revealed that the post-glacial assembly of bryophytes likely involved a complex history. Extant European populations originated from multiple sources with a contribution from allochthonous migrants representing 90-100% in about half of the 15 investigated species, which demonstrates the importance of LDD for the post-glacial recolonization of Europe by bryophytes and is unparalleled in any previous phylogeograhic study on other organisms.