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.

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].

 

 

 

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PalmTraits 1.0

Functional traits are characteristics of individuals, populations and species that determine their fitness, via their impacts on growth, survival and reproduction. Examples are leaf size, leaf thickness, fruit size, wood density…. Traits are great proxies for the ecology of species, and used extensively in macroecological and macroevolutionary research. PalmTraits 1.0 provides species-level trait data for all ca. 2500 palm (Arecaceae) species worldwide. The database is available from Dryad. The article in which we present the data was published in Scientific Data.

PalmTraits 1.0, Figure from the publication in the journal Scientific Data

What else did we (I and my collaborators) do with these data? For example, using average fruit size of palm species, we asked questions such as: Do large fruits co-occur with large-bodied animals that disperse these fruits? And: Does fruit size influence speciation rates via the interaction between fruits and fruit-eating and seed-dispersing animals? What happened to palms with large, ‘megafaunal’ fruits since the Quaternary extinctions of large-bodied animals?

Answers to these questions can be found in these publications:

Onstein, R.E. , Baker,W.J., Couvreur, T.L.P. , Faurby, S., Herrera-Alsina, L., Svenning, J.-C. & Kissling, W.D. (2018). “To adapt or go extinct? The fate of megafaunal palm fruits under past global change”. Proceedings of the Royal Society B 285: 20180882. [ABSTRACT] [PRESS RELEASE]

Onstein, R.E. , Baker,W.J., Couvreur, T.L.P. , Faurby, S. , Svenning, J.-C. & Kissling, W.D. (2017). “Frugivory-related traits promote speciation of tropical palms”. Nature Ecology & Evolution 1:1903–1911. [ABSTRACT] [DATA & CODE] [PRESS RELEASE] [BLOG]

However, the data can be used to answer many more questions, related to the ecology and evolution of palms. Species differ not only in their fruit sizes, but also in, for example, fruit colours, leaf structures and sizes, the presence or absence of spines, growth forms, plant height. In combination with distribution data and a phylogeny, we can now answer questions such as: when did these traits evolve? Where do species with these traits occur? Where do we find the most colourful fruits, and why? Where do species occur that have spines? Etcetera…

Humboldt in Journal of Biogeography

250 years ago (almost) Alexander von Humboldt was born, and became the “father of biogeography”. Journal of Biogeography decided to celebrate his birthday by publishing a ‘special issue‘ on Humboldt-related research, ranging from integrating geo- and biodiversity, to studying elevational and latitudinal diversity gradients and the impact of tectonism on biodiversity.

Portrait of Alexander von Humboldt by Joseph Karl Stieler, painted in 1843, and shows Humboldt with a copy of his major work, “Kosmos”, and is owned by the Prussian Palaces and Gardens Foundation Berlin‐Brandenburg.

I contributed to three studies that were published in this special issue:

The first one I described in more detail in the last post – on how fruit traits in tropical plant families may explain historical long-distance dispersal events. Read more in the press release (in English or Dutch) or publication: Onstein, RE, Kissling, WD, Chatrou, LW, Couvreur, TLP, Morlon, H, Sauquet, H. Which frugivory‐related traits facilitated historical long‐distance dispersal in the custard apple family (Annonaceae)? J Biogeogr.2019; 46: 1874– 1888. https://doi.org/10.1111/jbi.13552.

The second one was led by Suzette Flantua and introduces one of the ideas that emerged during her PhD at the University of Amsterdam, where we met and discussed this idea extensively over coffee: that some of the extraordinary diversity in paramós (and mountains more generally) may have resulted from a process she named ‘flickering connectivity’. It’s the balance between connectivity (of populations) and disconnection over time that may drive speciation. In this publication we quantified this connectivity through the Pleistocene in the northern Andes, by making use of a pollen-core and detailed temperature reconstructions. To illustrate these ideas, one of the authors made this amazing video. Read more in the press-release: (in English or Dutch) and publication: Flantua, SGA, O’Dea, A, Onstein, RE, Giraldo, C, Hooghiemstra, H. The flickering connectivity system of the north Andean páramos. J Biogeogr. 2019; 46: 1808– 1825. https://doi.org/10.1111/jbi.13607.

The third publication was led by Oskar Hagen, who is currently doing his PhD at the ETH in Zurich, Switserland (supervisor: Loïc Pellissier). He tries to understand how geological and biological processes interact in the generation of biodiversity (especially in mountains) – fitting very well in the Humboldt spirit. This publication addresses the origin of the Northern hemisphere mountain and Arctic floras, which have lots of lineages in common. Where did these lineages originate, and when? Where and when did cold ‘niches’ first emerge? To address these questions, we reconstructed cold niches throughout the Cenozoic by combining paleoclimate and paleoelevations, and combined these with species distribution data for cold-adapted taxa. Read more about it in the publication: Hagen, O, Vaterlaus, L, Albouy, C, et al. Mountain building, climate cooling and the richness of cold‐adapted plants in the Northern Hemisphere. J Biogeogr. 2019; 46: 1792– 1807. https://doi.org/10.1111/jbi.13653.

Fruits, animals and long-distance dispersal

In October 2015 Hervé Sauquet, Thomas Couvreur and I went on a field expedition in the rainforests of Borneo. Our aim was to collect plants belonging to the order Magnoliales, which includes the Annonaceae family. Annonaceae have beautiful flowers and tasty fruits (e.g. the sweetsop and soursop), worldwide there are ca. 2400 species, and they typically occur in tropical rainforests. Our expedition led, eventually, to a publication: “Which frugivory‐related traits facilitated historical long‐distance dispersal in the custard apple family (Annonaceae)?” published in Journal of Biogeography. and co-authored by Daniel Kissling, Lars Chatrou, Thomas Couvreur, Hélène Morlon and Hervé Sauquet. Read the press release from the University of Amsterdam here. A video of our Borneo expedition is available here.

How did Annonaceae colonise different continents or islands and their rainforests? How did they get there? To understand this, we need to look into how the plants are dispersed, which is via their fruits and seeds. On Borneo, our aim was therefore to collect the fruits and measure their ‘traits’ (e.g. fruit length, seed length, conspicuousness of fruit display). These traits are important because they attract animals to feed on the fruits and disperse the seeds. We expected that certain fruit-eating and seed-dispersing animals (i.e. frugivores) are more likely to perform intercontinental long-distance dispersal. For example, large-bodied animals (megafauna, such as elephants) and strong-flying birds (e.g. hornbills) have large home-ranges and/or can cross barriers (such as oceans), and therefore move across large distances. Because these animals prefer certain fruits (e.g. large fruits, or fruits with particular colours) we expect that these Annonaceae fruits may have been responsible for intercontinental long-distance dispersal, for example from South America to Africa, which happened repeatedly in the family throughout its history. Our results confirm these expectations.

Besides fun in the rainforest, this research was important to me because it was my first postdoc, I received a Swiss Mobility Fellowship to perform it, and it allowed me to live in Paris for a while and work with a couple of amazing researchers. I hope to continue working with these people on this tasty family in the future. For example, a lot more genetic and functional trait data need to be collected to be able to understand the complex eco-evolutionary dynamics that have led to the spectacular Annonaceae diversity.

From left to right, starting at the top: Rafflesia flower; Goniothalmus roseus fruits; Thomas, Renske & Hervé in the field; rainforest Borneo; Enicosantum sp. flower; the fieldwork team in action (twice).

 

 

Palms of Madagascar meeting in Leipzig

In the beginning of February, I organised a kick-off meeting for Laura Mendez‘ PhD project on “Genomic signatures of palms on Madagascar” – 3 days of discussions at iDiv in Leipzig (Germany). The team includes palm, frugivory and Madagascar experts from Kew Botanical Gardens, Aarhus University, University of Amsterdam, Bochum Botanical Gardens and iDiv – all important collaborators on Laura’s PhD project. The discussions ranged from deciding which species she will sample on Madagascar next summer, to clarifying the specific hypotheses and learning about historical demographic modelling techniques using Rad-seq data. A couple of very valuable and ‘fruitful’ days.

From left to right: John Dransfield, Chris Barratt, Daniel Kissling, Laura Mendez, Renske Onstein, Alex Zizka, Adriana Alzate, Wolf Eiserhardt, Wolfgang Stuppy, Jun Lim, Bill Baker.

iM2M Taproot video

You probably wonder: what the hell is a Taproot? It also took me a while after arriving at the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig. But, it’s basically another word for a ‘research theme’, although Taproots may have different aims. We introduce the aims, participants and projects part of the iM2M Taproot (integrating meso to macro scales) in this video.

Within the iM2M theme we aim to bridge micro, meso and macro spatial/temporal scales in ecology and evolution. If you are part of iDiv and you’d like to join our meetings (every two weeks on Wednesday mornings in Leipzig), or would like to receive more general Taproot updates, please let me know (renske.onstein@idiv.de).

With thanks to the iDiv media team!

The evolution of plants on Madagascar: who eats their fruits now that the giant lemurs have gone extinct?

I’m happy to announce that my proposal to make an outreach video about our work on Madagascar has been funded by the European Society for Evolutionary Biology (ESEB Outreach fund) and iDiv’s Female Scientists Career Fund.

Details will follow, but in short:

We aim to improve the understanding of evolutionary concepts (e.g. genetic connectivity, bottlenecks, speciation and extinction) at secondary schools. These concepts will be illustrated using video shootage from our fieldtrip to Madagascar (starring the new Evolution & Adaptation lab members Laura Mendez and Adriana Alzate!), as well as by use of animations. We study the evolutionary fate of Malagasy megafaunal-fruited plants (fruits > 3 cm) since the extinction of their primary seed dispersers: giant lemurs and elephant birds. Are these plants genetically adapting to new, smaller-bodied frugivores, or have they gone through genetic bottlenecks and are possibly facing extinction? The video will address these questions guided by the scientific and conservation activities performed by (female) researchers on Madagascar.

 

See you at Evolution in Montpellier?!

From 19-22 August 2018 I will attend the Evolution conference in Montpellier, France. I will present a poster on “Fruit colour as a driver for the evolution of trichromatic primate diversity” in S-33 Ecological models of macroevolution. Please visit me and / or my poster during the ‘Cocktail Poster Session 5.30pm –7.30pm’ on Tuesday 21st, or any other time!

 

Sneak preview….

The mutualism between fruits and frugivores is prominent in tropical rainforests, but to what extent fruits have influenced the macroevolution and macroecology of frugivores and their functional traits remains underexplored. Here, we hypothesize that trichromatic colour vision (i.e. the ability to distinguish green and red) in frugivorous primates has evolved as an adaptation to detect conspicuously coloured (i.e. reddish) fruits against a background of green foliage. The readily detection of these fruits as critical resources may have provided trichromatic primates a competitive advantage over dichromatic primates that cannot distinguish reds from greens.

To test this hypothesis, we combined global distribution, phylogenetic and colour vision data for >400 primate species with fruit colour data for >1700 palm and >80 fig species. Palms (Arecaceae) and figs (Ficus) are considered keystone resources for frugivores in tropical rainforests worldwide. We used structural equation modelling to show that the regional proportion of food plant species with conspicuously coloured fruits positively affects the diversity of trichromatic primates, but only in Africa. We show that this effect intensifies towards the tropics, following a hump-shaped relationship with food plant species richness. This suggests that the most species-rich places (i.e. rainforests) provide sufficient alternative food sources for primates, decreasing their dependence on conspicuous fruits. Overall, our results indicate that the consumption of palm and fig fruits could have been a driver for the diversification of trichromatic colour vision in African primates, and that food availability is an important determinant of frugivore diversity more generally.

 

New article published in Proceedings of the Royal Society B

Also see the press release from the University of Amsterdam.

Global change, such as climate changes, may have two outcomes with respect to biodiversity: species will adapt, or they will go extinct. In this article, we address this question from a historical perspective, focusing on the Quaternary (the last 2.6 Ma), a period characterised by rapid global changes. We show that in some parts of the world palm trees with very large fruits have adapted to global change, whereas in other parts they seem to have gone extinct.  The results were published in the journal Proceedings of the Royal Society B.

Global change – such as climate change, habitat fragmentations or the extinction of large-bodied animals , such as giant sloths, may force species to adapt or go extinct. In particular, plants with very large fruits that rely on large-bodied animals for the dispersal of their seeds may face a problem: can they adapt quick enough, or will global change drive them ultimately to extinction?

During the last 2.6 million years,  Latin American palms with the largest fruits seem to have gone extinct with increasing rates, whereas large-fruited palms in South-East Asian regions seem to be adapting by producing smaller fruits. Small enough to be eaten and dispersed by birds and bats. These were the results of Onstein and her team which consisted of researchers from the Netherlands, UK, France, Sweden and Denmark. They collected data for more than 2000 palm species across the globe.

Fruits need to become smaller

The absence of certain fruit-eaters, such as large hornbills, elephants or giant tortoises, may require plants with large, ‘megafaunal’ fruits to evolve ‘new’ fruits. This is similar to the selection by humans for fruits (such as papayas or mangos) to become bigger and bigger. However, instead of becoming bigger, these fruits naturally have to become smaller, to adapt to the small-bodied animals that are still there to disperse their seeds. A lack of dispersal may, alternatively, lead to their extinction.

‘Although it is difficult to see the long-term results of current global change, global change has been happening in the deep past as well, especially during the last 2,6 million years,’ says Onstein. ‘We therefore use the past as our experimental set-up to understand how current and future global change may affect these palms with very large fruits.’

Onstein thinks that the dramatic changes in climate, habitat fragmentation and megafauna extinctions that have happened in Latin America over the last 2.6 million years may have been the cause of the increasing extinction of palms. In South-East Asian regions, on the other hand, palm dispersal by flying animals such as birds and bats may have been important to escape the dramatic effects of global change. Palms seem to have had enough time to adapt to these flying animals by evolving smaller fruits.

The future of palms

How does the future of these palms with big fruits look like? There are still at least 220 palm species worldwide that bear these massive fruits larger than 4 cm in length. ‘Large-fruited plants have it increasingly difficult to survive in our human dominated world’, says Daniel Kissling, associate professor and senior author of the study. ‘The loss of large animals in tropical rainforests, e.g. due to hunting, illegal trade, and habitat loss, has a massive effect on tropical biodiversity. It leads to a reduced seed dispersal and less regeneration of these tall and massive plants. This has even the potential to significantly erode the carbon storage of tropical rainforest because large-fruited trees also store most carbon.’

The increasing human pressure and hunting of the still existing megafauna will certainly have cascading effects on the plants they feed on. Whether all palms will be able to adapt to the loss of large-bodied animal dispersers has to be seen.

Publication

Onstein RE, Baker WJ, Couvreur TLP, Faurby S, Herrera-Alsina L, Svenning J-C, Kissling WD. ( 2018 ). To adapt or go extinct? The fate of megafaunal palm fruits under past global change. Proceedings of the Royal Society B: Biological Sciences, 285, 20180882.