"Cosmopolitan" moss traveling the world on wind currents

Remarkable overlap of global wind patterns and biogeographic structure ​
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Ceratodon purpureus is one of the most widespread plants in the world. It can be found almost everywhere - on roofs, pavements, on a remote valley in Antarctica... In a recent study we investigated how and when this species managed to spread to almost every corner of the Earth, and to assess the level of connectivity between its globally widespread populations.

Applying phylogenetic, population genetic, and molecular dating analyses to a global sampling data set, we found several distinct and geographically structured populations within the chloroplast DNA of Ceratodon purpureus. In particular the most widespread of these lineages, in the Northern Hemisphere, the Southern Hemisphere and in the tropics were remarkably structured in worldwide, latitudinal "bands" (see red, blue and green specimens on the world map in the left figure above).

The biogeographic patterns of these most widespread populations imply that connectivity is strongly influenced by global atmospheric circulation patterns (see right figure above), with dispersal and establishment beyond these latitudinal bands less common. Biogeographic patterns were less clear within the nuclear DNA, with gene duplication likely hindering the detection of these.

Ceratodon purpureus. Illustration by Christiaan Sepp (Kops et al., 1868; Wikimedia Commons)

Old Lineages in Distinct Biogeographic Regions

We applied molecular dating analyses to assess the age of the populations. These indicated that the current population structure within the chloroplast DNA of C. purpureus has developed over the past six million years, with lineages diverging during the late Miocene, Pliocene, and Quaternary.

This surprising finding implies that the global distribution of a weedy, cosmopolitan species such as C. purpureus is mainly the result of a worldwide spread achieved by dispersal and establishment over hundreds of thousands to million-year timescales rather than high-frequency long-distance dispersal events, as would be expected for a highly ruderal species.



Drivers of Dispersal and Establishment

As C. purpureus s.l. is a weedy species, characteristically found in a wide range of dry and disturbed habitats, an increase in environmental (e.g. glacial, fire-influenced and, more recently, anthropogenic) disturbances could have aided its spread across the globe.

The main distribution of C. purpureus, occupying the vast areas of the temperate regions (particularly clades V-VII), became established throughout the late Pliocene and Quaternary (see time-calibrated phylogeny on the right). This was a period of high disturbance globally, including global cooling and repeated glacial periods (see global surface temperature estimated from Hansen et al., 2013 in the same figure). It is likely that repeated glacial disturbance provided favorable conditions for the spread and population expansion of C. purpureus in high latitude areas of both hemispheres.

Time-calibrated phylogeny of Ceratodon purpureus, based on a concatenated cpDNA data (for more information see Fig. 5 in main study). Global surface temperature estimates (blue and solid line representing temperature variations and a 500 kyr smoothed resolution, respectively), reproduced from Hansen et al. 2013, are provided below.

Repeated glacial disturbance, such as occurred in the Antarctic pictured above, has likely been favourable for the spread of the ruderal moss species Ceratodon purpureus.

Additionally, the rise of modern flammable grass-, shrub- and woodlands (late Miocene onwards with peak origins in late Pliocene; Bond, 2015) could have promoted the spread of C. purpureus, as the species is also frequently found in fire-influenced habitats (it is even called “Fire Moss” as a common name in English). Furthermore, in the recent post-quaternary period, the origin and expansion of urban environments provided major sources of anthropogenically influenced disturbance potentially favorable to C. purpureus.

Multiple Antarctic Colonizations, Including an Ancient Lineage

We found at least three dispersal events to the Antarctic (see clades I, V and VI above). This reveals that Antarctica is not as isolated as is often assumed for spore-dispersed organisms (e.g. also seen in the Antarctic moss Chorisodontium aciphyllum; Biersma et al., 2018a).
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However, the analyses also revealed one old Antarctic clade (I), possibly isolated on the continent since the late Miocene or early Pliocene. Although more extensive sampling may be required to fully assess whether clade I is limited to Antarctica, its apparent ancient isolation suggests it may be a remnant lineage that has survived past glaciations in the maritime Antarctic in situ. 

Molecular, phylogenetic and biogeographic studies also suggest in situ survival for many groups of terrestrial fauna in Antarctica throughout the Quaternary, Neogene and even Paleogene (see Convey et al., 2008, 2009, 2020, and references therein). Recently, increased evidence has also been found of million-year persistence of the Antarctic flora, e.g. several endemic species of Schistidium (Biersma et al., 2018b), and Bryum argenteum (Pisa et al., 2014). Here, our data indicate that at least one lineage (I) of C. purpureus may also have had a long-term Antarctic presence in situ.


Relevance for other organisms and evolutionary studies

Our general findings may also be relevant to understanding global environmental influences on the biogeography of other organisms with microscopic propagules (e.g., spores) dispersed by wind. The findings may also be of relevance to further evolutionary studies on bryophytes, as C. purpureus is commonly used as a model organism in genetic, physiological, and developmental studies, in particular for studying the evolution of developmental processes in bryophytes (e.g. McDaniel et al., 2007, and references therein; Szövényi et al., 2014). For this type of developmental research, good baseline knowledge on the evolutionary history and global biogeography of a species is fundamental, for instance, for underpinning interpretation of crossing experiments, trait mapping and marker discovery, and controlling for demographic or population effects. The matrilineal biogeographic structure identified here therefore provides a useful framework for future genetic and developmental studies on bryophytes.

​For more information see: 
Biersma, E.M., Convey, P., Wyber, R., Robinson, S.A., Dowton, M., Van De Vijver, B., Linse, K., Griffiths H. & Jackson, J.A. (2020) Latitudinal biogeographic structuring in the globally distributed moss Ceratodon purpureus. Front. Plant Sci. 11:502359.  https://doi.org/10.3389/fpls.2020.502359
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References:
Biersma, E. M., Jackson, J. A., Bracegirdle, T. J., Griffiths, H., Linse, K., Convey, P. (2018a). Low genetic variation between South American and Antarctic populations of the bank−forming moss Chorisodontium aciphyllum (Dicranaceae). Polar. Biol. 41, 599–610. doi: 10.1007/s00300-017-2221-1
Biersma, E. M., Jackson, J. A., Stech, M., Griffiths, H., Linse, K., Convey, P. (2018b). Molecular data suggest long-term in situ Antarctic persistence within Antarctica’s most speciose plant genus, Schistidium. Front. Ecol. Evol. 6:77. doi: 10.3389/fevo.2018.00077
Bond, W. J. (2015). Fires in the Cenozoic: a late flowering of flammable ecosystems. Front. Plant Sci. 5:749. doi: 10.3389/fpls.2014.00749
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Kops, J., Hartsen, F. A., van Eeden, F. W. (1868). Flora Batava, of Afbeeldingen en Beschrijving van Nederlandsche gewassen. XIII Deel 13(Amsterdam, the Netherlands: J. C. Sepp en Zoon).
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Pisa, S., Biersma, E. M., Convey, P., Patiño, J., Vanderpoorten, A., Werner, O., et al. (2014). The cosmopolitan moss Bryum argenteumin Antarctica: recent colonisation or in situ survival? Polar. Biol. 37, 1469–1477. doi: 10.1007/s00300-014-1537-3
Szövényi, P., Perroud, P. F., Symeonidi, A., Stevenson, S., Quatrano, R. S., Rensing, S. A., et al. (2014). De novo assembly and comparative analysis of the Ceratodon purpureus transcriptome. Mol. Ecol. Resour. 15, 203–215. doi: 10.1111/1755-0998.12284