A week with Shipley



Wageningen University, credit: JD Santillana-Ortiz

Last week I traveled back to my scientific roots (Wageningen University) to participate in a course on Structural Equation Modeling (SEM) given by Bill Shipley (he is particularly well known from his book on ‘Cause and Correlation in Biology‘). Structural Equation Models can be used to evaluate the sequence of variables affecting each other, and whether the underlying data supports such a sequence of events (also called path-models). For example – ecosystem functions (e.g. productivity and decomposition) can be affected by the biomass of the vegetation, and this can be affected again by the age of the plot (e.g. during succession) (Lohbeck et al. 2015).


some notes…

As an evolutionary ecologist I was a  bit of a misfit in the group. The group was dominated by Dutch PhD students and professors working in ecology (e.g. functional ecology, community assembly, soil science). They often collect data from plots; data which fit perfectly well in a structural equation model. My data did not – for a couple of reasons. My ‘plots’ are fossil assemblages (species richness = count data, problem 1), collected during the Cenozoic (different time scales, problem 2) and the variables we have are often not assemblage-specific but biased by time, and not normally distributed (e.g. CO2 concentration, temperature, latitude). On the positive side – I have a large sample size (N=666), which is necessary to have enough power to run these SEMs. So how can I test what factors directly and indirectly affect biodiversity (species richness)?

The solution. There is a solution. If your data is spatially, or phylogenetically biased, if your variables are not normally distributed, if you deal with binary/categorical/count data, if you have a nested design… The solution is the d-separation test. (d-sep cannot deal with ‘latent’ variables, e.g. unmeasured variables which may be important for the model).

d-separation in 6 steps:

  1. your hypothetical model (DAG: “Directed Acyclic Graph” avoid feedback loops in the model!) (for simplicity: A<- B <- C)
  2. write down each pair not connected by an arrow (in our example only AC)
  3. causal parents of these? (i.e. causal parent of A = B and of B = C. In our example of AC there is just one causal parent: B)
  4. run a suitable linear model/generalized linear model/PGLS/mixed model in which you test the effect of your pair variables, conditioned on the parent variables, in our example, of C on A conditioned on B (A ~ B + C)
  5. sum the probabilities (p values) of the slope coefficients of the regressions (in this case only one regression model was run, and we asses the coefficient of C and it’s p-value)
  6. calculate the C-statistic: -2 * ln (the sum calculated in step 5) and compare this to a Chi-square distribution. The degrees of freedom are calculated by 2* the number of regressions run (in our case 2 degrees of freedom). If p>0.05, you cannot reject you hypothesized model. If p<0.05 your data do not support the model.


    All analyses can be performed in R using packages ggm and lavaan. credit: JD Santillana-Ortiz

Thanks to the d-separation test we, evolutionary biologist, can still test for causal relationships in our data, even if these data are far from ‘perfect’ or complete. It provides great potential for the field of phylogenetic comparative methods. But how exactly I’m not sure yet….


Madelon Lohbeck, Lourens Poorter, Miguel Martínez-Ramos, and Frans Bongers 2015. Biomass is the main driver of changes in ecosystem process rates during tropical forest succession. Ecology 96:1242–1252. http://dx.doi.org/10.1890/14-0472.1

Fieldwork Borneo: the movie


The research team (left to right, top to bottom): Jeisin Jumian, Renske Onstein, Hervé Sauquet, Thomas Couvreur, Postar Miun, Joel Dawat, Tawadong Tangah, Aloysius Laim

To study and collect fruits, flowers and leaves of Magnoliales species, Hervé Sauquet, Thomas Couvreur, and I traveled to Sabah, Borneo. We just came back from a very successful trip in which we were amazed by the diversity of Magnoliales in the (mainly lowland) rainforests, and in particular the diversity of flowers and fruits of species belonging to the Annonaceae and Myristicaceae families. These collections wouldn’t have been possible without the help and expertise of our local team from the Forest Research Center (Sabah Forestry Department) in Sepilok.

For a short (informative and entertaining) summary of this trip, watch the video I made.



frugivory in the Atlantic rainforest, Brazil

I am currently doing a postdoc in the Sauquet lab at the Université Paris-Sud. In collaboration with Daniel Kissling, Hélène Morlon, Thomas Couvreur, Lars Chatrou and Hervé Sauquet, I study “Frugivory, functional traits and the diversification of a tropical angiosperm family: Annonaceae (Magnoliales)”.

For a 1 minute summary of the project- watch this video.

In short –

Frugivory (i.e. fruit-eating and seed dispersal by animals) is ubiquitous in tropical ecosystems, but the role that frugivores have played in the macroevolution of species-rich tropical plant families remains largely unexplored. This project will investigate how plant traits relevant to frugivory (e.g. fruit size, fruit color, fruit shape, understory/canopy growth form, etc.) are distributed within the angiosperm family of custard apples (Annonaceae), how this relates to diversification rates, and whether and how it coincides with the global biogeographic distribution of vertebrate frugivores (birds, bats, primates, other frugivorous mammals) and their ecological traits (e.g. diet specialization, body size, flight ability, etc.). Annonaceae are particularly suitable because they are well studied, species-rich (ca. 2400 species), characteristic in all tropical rainforests, and dispersed by most groups of vertebrate seed dispersers. Using a phylogenetic framework and functional trait and species distribution data we will test (i) how fruit trait variability relates to phylogeny and other aspects of plant morphology (e.g. leaf size, plant height, growth form, floral traits) and animal dispersers and their traits, (ii) to what extent interaction-relevant plant traits are related to diversification rates, and (iii) whether geographic variability in fruit traits correlates with the biogeographic distribution of animal dispersers and their traits.

NESCent video: Convergence in Mediterranean-Type Ecosystems

P1040772 (800x600)

Mediterranean shrubland in Western Australia

Why do plants in geographically distinct areas sometimes look so similar, even though they are different species, and have had different evolutionary histories? This may be, because they have evolved similar morphological features, or ‘adaptations’, in response to the similar environmental conditions in these areas. This is called ‘convergent evolution’. Convergent evolution may therefore explain why the five Mediterranean-type ecosystems of the world (California, central Chile, the Mediterranean Basin, the Cape and South and Southwestern Australia) have such a similar appearance, dominated by highly branched, woody shrubs with small sclerophyllous leaves. The similar environmental conditions in these regions – the typical ‘Mediterranean’ climate, very dry summers and fire – may have selected for these typical traits, independently in all five Mediterranean areas. However, the five regions show also considerable differences, such as absence of fire in Chile, and very poor soils (low in nutrients) in the Cape and Australia. This may explain why plants in the Cape and Australia are particularly ‘sclerophyllous’  – i.e. these sclerophyllous traits help to conserve their nutrients.

Being well adapted to your environment may decrease your chance to go extinct, and may allow for high rates of diversification, and the accumulation of species over long periods of time. These Mediterranean-type ecosystems indeed are very species-rich, and many species can co-exist in these systems. The evolution of these sclerophyllous traits in the Cape and Australia may therefore also partly explain why these systems are so diverse and species-rich, and became biodiversity ‘hotspots’ of the world.

I made a video about these concepts for the NESCent evolution film festival 2015, with help of my colleagues Guy Atchison (presenter) and Lorena Ament (illustrator). The video was screened at the Evolution meeting in Guarujá, Brazil, in June 2015.

Don’t miss this month’s New Phytologist!


What are evolutionary radiations, what can trigger them, where do we find them, and how can we test for them using molecular (DNA) sequence data and fossils?

This month the journal New Phytologist published a special issue on ‘evolutionary plant radiations’ – and I contributed to three of the papers in this issue: one on classifying the correlates of evolutionary radiations (“On the complexity of triggering evolutionary radiations” by Yanis Bouchenak-Khelladi, Renske E. Onstein, Yaowu Xing, Orlando Schwery and H. Peter Linder), one on radiations in mountain habitats and the interaction with sclerophyllous leaves (“As old as the mountains: the radiations of the Ericaceae” by Orlando Schwery, Renske E. Onstein, Yanis Bouchenak-Khelladi, Yaowu Xing, Richard J. Carter and Hans Peter Linder) and one on diversification of the enigmatic orchid genus Ophrys (“Multiple shifts to different pollinators fuelled rapid diversification in sexually deceptive Ophrys orchids” by Hendrik Breitkopf, Renske E. Onstein, Donata Cafasso, Philipp M. Schlüter and Salvatore Cozzolino). And the best is: I took the cover picture, which shows Erica verticillata in Kirstenbosch National Botanical Garden in Cape Town – Table Mountain can be seen in the background.





The moment is finally there…

Have you always wondered why there are so many different species of angioPhDdefence R.E.Onsteinsperms? Why Mediterranean-type ecosystems have such a floristic diversity? And why species in these systems often look very similar to each other, even though they are not related?

I have been wondering this during the last 4 years in which I worked on my PhD thesis, and found some exciting insights…

Phylogenetic comparative methods are a powerful tool to understand which factors may drive the evolution and diversification of lineages across space and time. Angiosperms have a certain flexibility in their evolution of traits, and seem to keep on ‘reinventing’ themselves. These ‘functional traits’ have enabled them to colonize all major terrestrial biomes, and even become the dominant elements in most of these systems.

Everyone is invited to come to my PhD thesis defence on the 2nd of June 2015 at 15h in the Botanical Garden in Zurich.


Cats, dogs, Darwin’s finches and cichlid fish

I recently had the funny thought that the evolution of classical cases of ‘adaptive radiations’, such as the Darwin’s finches and the cichlid fishes, are very similar to the evolution of domesticated animals, such as dogs and cats. With the only difference that we talk about different ‘breeds’ when it comes to cats and dogs, and different ‘species’ (most of the time) in case of finches and cichlids. Nevertheless, both categories show the spectacular morphological, phenotypic evolution typical for adaptive radiation.

Dog Breeds

Dog breeds of the world


Typical for adaptive radiation in the classical sense is that the group shows a very fast rate of evolution, resulting in many different species, supposedly because of strong selection pressure by the environment. In case of the finches this has resulted in species specialized on different food sources, and consequently showing a spectacular change in beak morphology, where ground finches have large beaks for cracking seeds, and warbler finches have more elongated small beaks for spearing insects, for example. The cichlids – those occurring in the African Great Lakes- seem to adapt to different lake features and show disparity in body sizes and colors. This last feature contributes to strong sexual selection, where females of one species are more attracted to the color pattern of the male of the same species, than to the color pattern of another species’ male. Clearly, if we stick to mating with the same species, this will accelerate the speciation process, because ‘gene flow’ between non-species will inhibit the evolution of new species.

They recently discovered the underlying genetics of Darwin finches and the genes coding for their classical beak morphologies. Interestingly, although these finches all look very different, there was “extensive sharing of genetic variation among populations […], particularly among ground and tree finches, with almost no fixed differences between species in each group” (Lamichhaney et al. 2015). This suggests that, although there is selection on the genes coding for beak morphology, there are not much genetic differences between species. This raises the question: are they really different species? Or are they in the process of becoming different species?

What about the parallel to our cats and dogs? In this example we, humans, are the selective environment, selecting for genes coding for long fur / short fur, pointy ears / floppy ears, long tail / short tail, big dog / small dog, etcetera, which has resulted in the spectacular morphological diversity of domesticated dogs and cats. Funnily, these breeds are still the same species or subspecies (Canis lupus familiaris for the dog, and Felis catus for cats). Why don’t we call these different forms different species, resulting from adaptive (human) radiations? Or, perhaps better, are Darwin’s finches and cichlid fish, without much genetic differentiation, really different species?


Sangeet Lamichhaney, Jonas Berglund, Markus Sällman Almén, Khurram Maqbool, Manfred Grabherr, Alvaro Martinez-Barrio, Marta Promerová, Carl-Johan Rubin, Chao Wang, Neda Zamani, B. Rosemary Grant, Peter R. Grant, Matthew T. Webster, Leif Andersson. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature, 2015; DOI: 10.1038/nature14181