Evolutionary radiations in the species-rich mountain genus Saxifraga L.

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Abstract

Background

A large number of taxa have undergone evolutionary radiations in mountainous areas, rendering alpine systems particularly suitable to study the extrinsic and intrinsic factors that have shaped diversification patterns in plants. The species-rich genus Saxifraga L. is widely distributed throughout the Northern Hemisphere, with high species numbers in the regions adjacent to the Qinghai-Tibet Plateau (QTP) in particular the Hengduan Mountains and the Himalayas. Using a dataset of 297 taxa (representing at least 60% of extant Saxifraga species), we explored the variation of infrageneric diversification rates. In addition, we used state-dependent speciation and extinction models to test the effects of geographic distribution in the Hengduan Mountains and the entire QTP region as well as of two morphological traits (cushion habit and specialized lime-secreting glands, so-called hydathodes) on the diversification of this genus.

Results

We detected two to three rate shifts across the Saxifraga phylogeny and two of these shifts led to radiations within two large subclades of Saxifraga, sect. Ciliatae Haworth subsect. Hirculoideae Engl. & Irmsch. and sect. Porphyrion Tausch subsect. Kabschia Engl . GEOSSE analyses showed that presence in the Hengduan Mountains had a positive effect on diversification across Saxifraga. Influence of these mountains was strongest in Saxifraga sect. Ciliatae subsect. Hirculoideae given its pronounced distribution there, and thus the radiation in this group can be classified at least partially as geographic. In contrast, the evolution of the cushion life form and lime-secreting hydathodes had positive effects on diversification only in selected Saxifraga sections, including sect. Porphyrion subsect. Kabschia. We therefore argue that radiation in this group was likely adaptive.

Conclusions

Our study underlines the complexity of processes and factors underpinning plant radiations: Even in closely related lineages occupying the same life zone, shifts in diversification are not necessarily governed by similar factors. In conclusion, alpine plant radiations result from a complex interaction among geographical settings and/or climatic modifications providing key opportunities for diversification as well as the evolution of key innovations.

Electronic supplementary material

The online version of this article (doi:10.1186/s12862-017-0967-2) contains supplementary material, which is available to authorized users.

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Most cited references 58

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Trends, rhythms, and aberrations in global climate 65 Ma to present.

J Zachos, M. Pagani, L. Sloan … (2001)

Since 65 million years ago (Ma), Earth's climate has undergone a significant and complex evolution, the finer details of which are now coming to light through investigations of deep-sea sediment cores. This evolution includes gradual trends of warming and cooling driven by tectonic processes on time scales of 10(5) to 10(7) years, rhythmic or periodic cycles driven by orbital processes with 10(4)- to 10(6)-year cyclicity, and rare rapid aberrant shifts and extreme climate transients with durations of 10(3) to 10(5) years. Here, recent progress in defining the evolution of global climate over the Cenozoic Era is reviewed. We focus primarily on the periodic and anomalous components of variability over the early portion of this era, as constrained by the latest generation of deep-sea isotope records. We also consider how this improved perspective has led to the recognition of previously unforeseen mechanisms for altering climate.

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Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation.

Daniel L. Rabosky, Francesco Santini, Jonathan Eastman … (2013)

Several evolutionary theories predict that rates of morphological change should be positively associated with the rate at which new species arise. For example, the theory of punctuated equilibrium proposes that phenotypic change typically occurs in rapid bursts associated with speciation events. However, recent phylogenetic studies have found little evidence linking these processes in nature. Here we demonstrate that rates of species diversification are highly correlated with the rate of body size evolution across the 30,000+ living species of ray-finned fishes that comprise the majority of vertebrate biological diversity. This coupling is a general feature of fish evolution and transcends vast differences in ecology and body-plan organization. Our results may reflect a widespread speciational mode of character change in living fishes. Alternatively, these findings are consistent with the hypothesis that phenotypic 'evolvability'-the capacity of organisms to evolve-shapes the dynamics of speciation through time at the largest phylogenetic scales.

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Model inadequacy and mistaken inferences of trait-dependent speciation.

Daniel L. Rabosky, Emma Goldberg (2015)

Species richness varies widely across the tree of life, and there is great interest in identifying ecological, geographic, and other factors that affect rates of species proliferation. Recent methods for explicitly modeling the relationships among character states, speciation rates, and extinction rates on phylogenetic trees- BiSSE, QuaSSE, GeoSSE, and related models-have been widely used to test hypotheses about character state-dependent diversification rates. Here, we document the disconcerting ease with which neutral traits are inferred to have statistically significant associations with speciation rate. We first demonstrate this unfortunate effect for a known model assumption violation: shifts in speciation rate associated with a character not included in the model. We further show that for many empirical phylogenies, characters simulated in the absence of state-dependent diversification exhibit an even higher Type I error rate, indicating that the method is susceptible to additional, unknown model inadequacies. For traits that evolve slowly, the root cause appears to be a statistical framework that does not require replicated shifts in character state and diversification. However, spurious associations between character state and speciation rate arise even for traits that lack phylogenetic signal, suggesting that phylogenetic pseudoreplication alone cannot fully explain the problem. The surprising severity of this phenomenon suggests that many trait-diversification relationships reported in the literature may not be real. More generally, we highlight the need for diagnosing and understanding the consequences of model inadequacy in phylogenetic comparative methods.

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Author and article information

Contributors

J. Ebersbach:

ORCID: http://orcid.org/0000-0002-2528-8325

ebersbach.jana@gmail.com

Journal

Journal ID (nlm-ta): BMC Evol Biol

Journal ID (iso-abbrev): BMC Evol. Biol

Title: BMC Evolutionary Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2148

Publication date (Electronic): 25 May 2017

Publication date PMC-release: 25 May 2017

Publication date Collection: 2017

Volume: 17

Electronic Location Identifier: 119

Affiliations

[1 ]ISNI 0000 0001 2230 9752, GRID grid.9647.c, Department of Molecular Evolution and Plant Systematics & Herbarium (LZ), Institute of Biology, , Leipzig University, ; Johannisallee 21–23, D-04103 Leipzig, Germany

[2 ]ISNI 0000 0001 2230 9752, GRID grid.9647.c, , German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, ; Deutscher Platz 5e, D-04103 Leipzig, Germany

Author information

J. Ebersbach http://orcid.org/0000-0002-2528-8325

Article

Publisher ID: 967

DOI: 10.1186/s12862-017-0967-2

PMC ID: 5445344

PubMed ID: 28545386

SO-VID: 27c85540-6cbc-46e4-b099-d954155bed91

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 18 November 2016

Date accepted : 12 May 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;

Award ID: MU 2934/3-1

Funded by: Hessisches Ministerium für Wissenschaft und Kunst (DE)

Award ID: LOEWE _ Landes-Offensive zur Entwicklung Wissenschaftlich-oekonomischer Exzellenz

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ScienceOpen disciplines: Evolutionary Biology

Keywords: evolutionary radiations,alpine habitats,saxifraga,diversification rates,key innovations,hengduan mountains

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ScienceOpen disciplines: Evolutionary Biology

Keywords: evolutionary radiations, alpine habitats, saxifraga, diversification rates, key innovations, hengduan mountains

Evolutionary radiations in the species-rich mountain genus Saxifraga L.

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Most cited references 58

Trends, rhythms, and aberrations in global climate 65 Ma to present.

Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation.

Model inadequacy and mistaken inferences of trait-dependent speciation.

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