Environmentally driven extinction and opportunistic origination explain fern diversification patterns - PubMed (original) (raw)
Environmentally driven extinction and opportunistic origination explain fern diversification patterns
Samuli Lehtonen et al. Sci Rep. 2017.
Abstract
Combining palaeontological and neontological data offers a unique opportunity to investigate the relative roles of biotic and abiotic controls of species diversification, and the importance of origination versus extinction in driving evolutionary dynamics. Ferns comprise a major terrestrial plant radiation with an extensive evolutionary history providing a wealth of modern and fossil data for modelling environmental drivers of diversification. Here we develop a novel Bayesian model to simultaneously estimate correlations between diversification dynamics and multiple environmental trajectories. We estimate the impact of different factors on fern diversification over the past 400 million years by analysing a comprehensive dataset of fossil occurrences and complement these findings by analysing a large molecular phylogeny. We show that origination and extinction rates are governed by fundamentally different processes: originations depend on within-group diversity but are largely unaffected by environmental changes, whereas extinctions are strongly affected by external factors such as climate and geology. Our results indicate that the prime driver of fern diversity dynamics is environmentally driven extinction, with origination being an opportunistic response to diminishing ecospace occupancy.
Conflict of interest statement
The authors declare that they have no competing interests.
Figures
Figure 1
Analytical workflow developed for this study. We used neontological (green) and palaeontological (grey) data sources to model fern diversification dynamics. In the first round of analyses (pale blue) we summarized climatic layer information for each species, built a time-calibrated molecular phylogeny, and estimated origination and extinction times of fern genera using the fossil record. These analyses provided data for the final analyses (blue) where we tested whether the rate variation observed in the phylogeny and fossil record were correlated with various candidate biotic and abiotic factors, niche and molecular evolution, and life form. We also estimated data compatability between the neontological and palaeontological models. Maps of modern world were created using QGIS v. 2.0.1 (
) and the statistical programming language R, the paleomap is based on PALEOMAP Global Plate Tectonic Model and was created using Adobe Photoshop CC 2015, PointTracker and QGIS v. 2.0.1 (
).
Figure 2
Diversification dynamics of ferns through time. (a) The green diagrams show the diversity dynamics of fern genera that were assigned to higher taxa (orders) inferred from the fossil record (Supplementary Table 1), plotted above a time-calibrated molecular phylogeny collapsed to the genus level. Pale green indicates the estimated maximum diversity (95% HPD), dark green the estimated minimum (95% HPD), and intermediate green the estimated mean diversity. (b) Diversification rate shifts identified from a species-level phylogeny for speciation and (c) extinction rates. Some important higher taxa (orders in b and families in c) are labelled and epiphytic species indicated by dots.
Figure 3
Characterisation of the studied fern genera. (a), Estimated ages of fern genera present in both molecular and fossil data sets (n = 76). Molecular age interval represents 95% HPD combining the stem and crown group nodes. Genera with congruent age estimates between the two methods are shown in blue and non-overlapping estimates in red. (b) Representative taxa from the analyses that include both living and extinct relatives: Gleicheniales: Dicranopteris flexuosa. (c) Cyatheales: Dicksonia antarctica. (d) Polypodiales: Polystichum acrostichoides.
Figure 4
Paleoenvironmental correlates and diversification dynamics of ferns. (a) Correlation parameters (G_i_) for fern originations and extinctions with darker colours indicating higher shrinkage weight (red for negative, blue for positive correlation). Significant correlations (shrinkage weight >0.5) are indicated by asterisks. (b) Origination (left panel) and extinction (right panel) rates through time as estimated from the fossil record using the BDS model and (c) by the MBD model. The clear similarity between origination and extinction dynamics estimated under the two models indicate that the MBD model and the set of variables tested here can adequately recover the rates inferred under the BDS model disregarding potential correlates.
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References
- Niklas KJ, Tiffney BH, Knoll AH. Patterns in vascular land plant diversification. Nature. 1983;303:614–616. doi: 10.1038/303614a0. - DOI
- Rothwell GW. Pteridophytic evolution: an often underappreciated phytological success story. Rev. Palaeobot. Palynol. 1996;90:209–222. doi: 10.1016/0034-6667(95)00084-4. - DOI
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