Trait flexibility leading to angiosperm success

As part of the “Tansley Medal” competition of the journal New Phytologist, I was asked to write a short (max 2500 words) Tansley Insight article. I applied for the competition a year ago, and was informed last April that I was short-listed. This pushed me to finally write this review, of which the topic dates from my PhD times.

I did my PhD at the University of Zurich as part of the ‘Cenozoic Angiosperm Radiation’ (CAR) project led by Prof. Peter Linder (who recently retired). The CAR team included several people, among them Colin Hughes, Yaowu Xing, Yanis Bouchenak-Khelladi and Erik Koenen. We would have Tuesday afternoon beers for several years to discuss ideas and projects. The main aim was to understand angiosperm radiations from phylogenies, fossils and functional traits, and we managed to tackle this question in several angiosperm clades, such as Fagales, Rhamnaceae, Proteaceae and Ericaceae. The emergent patterns across clades showed that radiations, or evolutionary diversification, is often the result of the intricate interaction between traits and environments. Screen Shot 2019-12-19 at 11.52.01

What remained an unanswered question, to me at least, was why angiosperms seem to have managed to radiate much more than other plant clades, such as gymnosperms, and also why not all angiosperm clades do equally well (in terms of their diversification rate). This question is not new, it was already proposed by Darwin (his second ‘abominable mystery’) and reviewed by Crepet and Niklas in 2009.

What I propose in my review, is that angiosperms (compared with gymnosperms) and species-rich angiosperm lineages (compared with species-poor lineages) have had (1) many trait innovations, (2) many ecological opportunities that emerged during Cenozoic global changes and (3) ‘trait flexibility’ to explore the functional space of novel traits, allowing for rapid adaptation to novel environments. These three ‘ingredients’ combined could lead to increased diversification rates. I quantified the support for this idea by performing a systematic review across the literature for trait-dependent diversification rates (key innovations) and trait transition rates (trait flexibility). Indeed, it seems that although no trait consistently leads to radiation across angiosperms, certain lineages may be predisposed to evolve the right traits in the right place at the right time, suggesting trait flexibility. This may have a genetic basis, and may explain why angiosperms have risen to dominance in most terrestrial ecosystems during the Cenozoic (i.e., the last 66 million years).

Hopefully it’s good enough to win the Tansley Medal.

Reference:

Onstein, RE (in press). “Darwin’s second ‘abominable mystery’: trait flexibility as the innovation leading to angiosperm diversity” New Phytologist. [ABSTRACT].

 

 

 

Proteaceae and their success in open habitats

geb-cover-onstein-et-al-leucospermum-cordifolium

Leucospermum erubescens

In a recent study, published in the journal Global Ecology and Biogeography, we investigate the evolution of leaf morphologies and climatic niches in the Proteaceae family. Proteaceae is a Southern 20131216143659639-page-001Hemisphere family famous especially in Australia and South Africa for their impressive flowers and leaves. They are also tasty – the macademia nut belongs to the Proteaceae as well. Species in the Proteaceae family occur in all kinds of habitats, from montane forests to dry heathlands to tropical rainforests. During their evolution over millions of years, they managed to adapt to these variable and extreme habitats and climates, and their leaves may have helped them doing so. In this study we test whether open (e.g. mediterranean) and closed (e.g. tropical rainforest) habitats have selected for divergent leaf designs. We also show that the combination of certain leaf traits (e.g. small, sclerophyllous leaves with many teeth) in interaction with certain climatic niches (e.g. warm, dry, mediterranean) may increase diversification rates. This could explain some of the spectacular radiations within the family, for example inbanksia-speciosa-9_10-566x800 genus Banksia in Australia, or the Protea in Africa. Last, we show that there is more stochastic evolution of traits and niches in open habitats, which may explain some of the extreme forms and ‘misfits’ we find here. This “disparification” maybe even led to the process of reproductive isolation and speciation, roupala-longipetiolata-4_6-mtvia ecological divergence, and the ~1700 species of Proteaceae we find on Earth.

Onstein, R.E., Jordan, G.J., Sauquet, H., Weston, P.H., Bouchenak-Khelladi, Y., Carpenter, R.J., Linder, H.P. (2016). “Evolutionary radiations of Proteaceae are triggered by the interaction between traits and climates in open habitats.” Global Ecology and Biogeography 25 (10):1239–1251. doi: 10.1111/geb.12481

 

CAD: a macrofossil angiosperm database

Yaowu Xing and colleagues (Maria A. Gandolfo, Renske E. Onstein, David J. Cantrill, cadBonnie F. Jacobs, Gregory J. Jordan, Daphne E. Lee, Svetlana Popova, Rashmi Srivastava,Tao Su, Sergei V. Vikulin, Atsushi Yabe, and H. Peter Linder) just published an article presenting the CAD (Cenozoic Angiosperm Database): Testing the Biases in the Rich Cenozoic Angiosperm Macrofossil Record in International Journal of Plant Sciences. The database is available from http://www.fossil-cad.net/.

The angiosperms currently have approximately 350,000 species, but how have angiosperms achieved such a high diversity? This question has bothered evolutionary biologists for centuries. The fossil database allows us to understand diversity changes in the past. Especially for angiosperms little is known about the temporal dynamics of species, lineage diversification and richness. It is structured by site (geographical information for each fossil assemblage), geology (name, age, epoch and stages of the formation), taxon (identification reliability and nearest living relatives of each taxon) and taxonomy. We hope that researchers will use the database to understand macro-evolutionary processes in angiosperms – possibly combining data from the database with inferences made from molecular phylogenetics.

For any questions concerning the database, contact Yaowu: yxing (at) fieldmuseum.org.