The Disturbed Team: Are diversification rates across clades shifted by geo-climactic events in a predictable manner? (Grant)

Grant proposal

Conceptual framework

The aim of this study is to analyse and characterize the effect of different types of geo-climatic events in the shifts of diversification rates across taxa. Changes in diversification rates are the proximate mechanisms shaping current diversity. Yet, the factors responsible for changes in diversification rates are still understudied despite their importance in determining current diversity patterns. We expect geo-climatic events to cause either an increase or decrease in diversification rates, and that different types of geo-climatic events should produce different effects on diversification rates. More specifically, we want to characterize how climatic changes, the formation of mountain ranges, and the formation of islands affect diversification rates. In order to do this we will take a meta-analytical approach to quantify and characterize the effects of the above geo-climatic events across different taxa.

Specific Aims

  • Describing patterns of diversification rates.
  • Analyse the temporal patterns of diversification rates.
  • Determine if the magnitude and timing of the diversification rates can be associated with a particular type of geo-climatic event.
  • Characterize the phylogenetic signal that is associated with the different types of geo-climatic events (uplift of mountain ranges, changes in climatic conditions, creation of new islands)

Hypothesis 1:

  • Geo-climatic events explains the diversity patterns we find today


  1. We expect changes in diversification rates to show some degree of synchrony across taxa.
  2. We expect to encounter an association between diversification rate with a geo-climactic event, either on a global or local scale.

Hypothesis 2:

  • Different types and scales of events will cause different patterns of diversification rate shifts


  1. Formation of mountain ranges (e.g. Andean uplift ): should increase ecological opportunities and/or vicariance events that will produce an increase in diversification rates in a synchronous manner.
  2. Changes in environmental conditions (e.g. changes in water acidification) should decrease diversification rates in some groups, while diversification rates in other groups could increase. 
  3. Formation of islands (e.g. Galapagos islands) should increase diversification rate in a non-synchronous, but successive way, because diversification rates should be associated with the colonization capabilities of the different organisms. 


Understanding how different mechanisms shape patterns of diversity has always been one of the major research fields of evolutionary biologists. Recent patterns of species richness across clades reflect the balance between speciation and extinction rates over their evolutionary history [22]. Such patterns, however, are most probably driven not only by specific/ecological traits, but also by local and global scale environmental processes [21]. Many possible mechanisms for the evolution of these diversity patterns have been hypothesized, of which the most prevalent in the scientific literature are those related to the biogeography of lineages and species, and its correlation to latitudinal or depth gradients [2,13,18,28]. To explain these patterns, many ecological and evolutionary mechanisms have been proposed [21, 26]. However, it is highly unlikely that this process is driven by a single factor, being most likely driven by a complex net of biotic and abiotic interactions. As such, a better understanding for these biotic and abiotic interactions is of fundamental scientific importance. Furthermore, understanding the ecological and evolutionary drivers of the past is fundamental for predicting and hypothesizing the ecological consequences of environmental changes such as human-mediated climate change or habitat fragmentation.
A possible approach to this question is to compare diversification rates of different animal and plant lineages through time. Several models have been proposed to calculate diversification rates from phylogenetic trees. These models primarily rely on time-calibrated phylogenies [for reviews see 22,25]. There are still limits to this methodology; for example, the lack of data on extinct lineages could possibly bias the analysis [22]. However, even though we are currently unable to calculate “true” diversification rates, well-calibrated molecular phylogenies can still determine when diversification rate shifts have occurred [25]. By correlating these rate shifts with ecological or biogeographic changes, and looking at similar changes across a number of phylogenies, we can improve our knowledge of how environmental changes affect diversification rates. This is important because, now, we can improve our knowledge of how environmental changes affect diversification rates. Previous studies [11,24] of changes of paleo-environmental conditions have been correlated to shifts in speciation and extinction rates of all or most terrestrial or marine phyla. For example, if past mountains uplifts are associated with an increase of diversification rate.

Changes in diversification rates represent shifts in relative speciation and extinction rates. By identifying rate shifts that have occurred at a particular point in time, it is possible to establish if there are congruencies in the time that these changes occurs across different clades, both world-widely and locally. If a pattern is found, one might infer that it was caused by changes in the abiotic or biotic environment. By then looking at the fossil and geologic record, it will be possible to specify the event that caused changes in the environment. The use of this approach has a great potential to improve our understanding on the cause (abiotic/biotic) and effect (biotic) of current species distribution.

In our study, we will investigate whether the type of the geo-climatic event is associated with the magnitude and direction of diversification rate shifts. In the case of mountain uplifts, an increase in diversification rates is expected because species will be presented with novel ecological opportunities [11]. Conversely, changes in ocean acidification will probably affect clades differently, with extinction occurring in some clades and higher diversification rates occurring on other clades [15]. In the case of island formation, a successive increase in diversification rates can be expected as species colonize the islands and diversify [16].

Research Approach

Phylogeny Selection

In order to test our hypotheses, we will download molecular phylogenies from clades from across the plant and animal trees of life available in the published literature. While there is an abundance of recently published phylogenies in the literature, not all of these are appropriate for investigating our hypotheses. First, we will need to select ultrametric tree that have been calibrated with a molecular clock or fossils, or that node ages have previously been inferred. Second, we need phylogenies that span the geography and time of biogeographic and climactic events. These phylogenies will need to be for clades that originated before these events, so that signatures of diversification from within these clades can be detected. Third, we need phylogenies that are well enough resolved to be able to assign shifts of diversification rates to particular geographic areas. Finally, we need phylogenies for which we can reliably assign richness scores to all clades.

Diversification Rates

For each phylogeny, we will estimate rates of diversification and identify any significant shifts in diversification rates. We will model diversification using a stepwise AIC (MEDUSA; Alfaro et al. 2009), using an AIC cutoff of four [5]. We will fit both birth death and Yule models [25] for every node, cut both at the stem and node. The model combination with the highest likelihood score will be taken as the likelihood for that node. Once we have identified all of the nodes with rate shifts, we will extract the ages of the nodes, the best-fit model, and the rates of speciation, extinction (if applicable). We will infer the geographic location of the rate shift by reconstructing the ancestral range of the shift using maximum likelihood estimation based on ranges of extant taxa [Lagrange 23]. We will compile the locations, times, models and parameters for all rate shifts found (e.g. Table 1). We will then match these times and locations with geoclimactic events that may have occurred. In some cases, there may not be a geoclimactic event associated with the shift, and these will get put into a separate category.

Tabela1: Results of MEDUSA analyses for each rate shift, parameter estimates, clade designations and ages

Geoclimatic Associations

First, we will look for synchronous changes across clades by binning positive and negative rate shifts into five million year bins (Fig. 1), and separating them by terrestrial or marine, island or continental, and old world or new world. We will test whether these distributions are significantly different than the null (random uniform distribution) using the Kolmogorov-Smirnov test. We will further test for correlations between geo-climactic event types, locations, and diversification rates using a phylogenetic mixed model [MCMgimm10] with location and geo-climactic events as fixed effects, and phylogeny as a random effect.
Figure 1: The number of nodes with different diversification rates and estimated time that the lineage appeared. (A) If a geo-climatic change is associated with diversification rate, and (B) if a geo-climatic change is not associated with diversification rate.

Preliminary Results

To test possible diversification rates shifts we used MEDUSA on the following phylogenies: furnarids, corals, nymphalid butterflies and Darwin finches (Fig. 2).


Figure 2: Molecular calibrated phylogenies showing the nodes that were identified by MEDUSA as presenting significant shifts in diversification rates for: furnarids (A), corals (B), nymphalid butterflies (C), and Darwin finches (D).

Oven birds and wood creepers diversification rates

The Neotropical ovenbird-woodcreeper family (Furnariidae) is an avian group characterized by exceptionally diverse ecomorphological adaptations. We estimated diversification rates for the different clades within the tree using 105 species representing more than one third of all species in Furnariidae [12, Figure 2.A]. The species selected covered all major radiations of ovenbirds and woodcreepers as suggested by recent molecular studies.
The mean diversification rate for the ovenbird-wood-creeper clade was estimated as 0.15, while the estimated diversification rate for the different sub-clades varied between 0.05 and 0.22. The synallaxine clade was found to have the highest diversification rate (0.57). By comparing the age estimates calculated with the geo-climatic development of South America, it is evident that the radiation of synallaxine ovenbirds mainly took place during the last 15 Mya, which was a period when South America experienced a period of cooling and aridification. It is possible that the ability, and flexibility, in building vegetative nests in dense bushy vegetation, may have allowed the synallaxines to build up large populations during that time period and were therefore able to expand and diversify.

Coral diversification rates

Although using a somewhat comprehensive scleractinian phylogeny that incorporates molecular clock estimates to date [derived from 20], only three shifts in diversification rates were recovered upon the application of MEDUSA. Nonetheless, among them, two antagonistic diversification shifts around middle to late Cretaceous may be related to global scale events. Interestingly, one of these shifts – a decrease in diversification rate - is observed on a lineage that captures most of the scleractinian families that, nowadays, contain most of the zooxanthellate, shallow-water representatives (e.g. Faviidae, Mussidae, etc), whereas an increment of diversification rate is observed in a deep-water, azooxanthellate coral family (i.e. Flabellidae). These contrasting results may indicate that shallow-water, zooxanthellate forms may be more directly influenced by ocean acidification [for a review of ocean acidification events see ((bibcite Kiessling2011] than deep-water, azooxanthellate forms. As such, these results corroborate with the idea that the deep-water scleractinian lineages have persisted through several episodes of dramatic environmental changes (at least 4 ocean acidification) during the last 450 Mya [20]. However, whilst on evolutionary time scales the Scleractinia may be less vulnerable than is sometimes assumed, the short-term survival of shallow-water coral reefs as we know them is far less assured.

Nymphalid butterflies diversification rates

Butterflies of the family Nymphalidae are a very charismatic and appealing group of insects, with a long history as models for numerous evolutionary and ecological studies [3], such as for studies on selection [8], speciation [14], species boundaries [17], coevolution [4] and hybrid zones [7]. The higher taxonomy, systematics and phylogeny of Nymphalidae is well resolved, and it have been proposed that their major diversification followed the Cretaceous/Tertiary boundary extinction event [27].

We used the phylogeny proposed by Whalberg et al. [27] to apply our technique. We found 17 shifts in the rates of divergence within the group, including 10 increases and seven decreases in diversification rates. Eight shifts are observed in Neotropical groups (six increases and two decrease events in small clades). Within these eight shifts, four occurred between 35-45 Mya and four occurred between 23-11 Mya including one in a very speciose Andean genus. Three shifts occurred in clades distributed world widely and these were between 71-50 Mya, out of which there were two increases and one decrease in diversification rate. In the Paleotropic region three shifts occurred between 55-48 May, all of which decreased in diversification rate. The remaining two other changes were decreases in small clades in the Holoartic region. It seems that the changes can be separated in three events one at 70-50 Mya that had world-wide impact, one at 35-45 Mya and a more recent decrease around 20-10 Mya both impacting Neotropical Biota.

Finches diversification rates
The Darwin's Finches are a classic example of an adaptive radiation, with many seminal papers on speciation, morphological evolution, and ecological specialization [9]. While the phylogenetic position of the clade was previously only hypothesized, the group was recently shown to be a member of the tanagers [family Thraupidae; 6]. The species in this clade, called Tholospizae, are residents of the Galapagos and Cocos Islands, and come from a clade where the other members reside on islands in the Caribbean or on the mainland of South American [6]. After applying MEDUSA to the Tholospiza phylogeny, we identified one significant shift in diversification rate, for the clade including species from the genera Geospiza, Camarhynchus, and Pinaroloxias, most of the species termed "Darwin's finches". We infer this shift to have occurred 1.5 million years ago, well after the formation of the Galapagos island archipelago, which formed about 4.5 million years ago [19]. While other species in the clade are associated with islands, the Caribbean islands are located much closer to the mainland. Unlike the isolated Galapagos Islands, it is more likely that dispersal events may have occurred multiple times to the Caribbean islands, preventing a single increase in diversification rate.

Broader Impacts

This study will be conducted by a multidisciplinary network of international researchers from four different countries (Brazil, Poland, USA and Germany). During the course of the research we will train undergraduate, masters and Ph.D students from different countries and institutions, also two post docs will be hired. Our methodology will allow us to compare various geo-climatic events and their effects upon diversification rates. This will provide us with the necessary information to evaluate which are the mechanisms responsible for the generation of diversity patterns observed today. Moreover, this study will also provide fundamental data that will allow us to predict and hypothesize the possible ecological consequences of long-term anthropogenic impacts such as climate change. Thus, providing relevant information to biodiversity protection programs and to policy makers.

Glossary words

Diversification rates
Extinction rates
Molecular clock

1. Alfaro, M. E., Santini, F., Brock C., Alamillo, H. Dornburg, A., Rabosky, D. L., Canevale, G. and L. J. Harmon (2009). Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proceedings of the National Academy of Sciences 106, 13410-134414.
2. Arita, H.T. and E. Vázquez-Domínguez (2008). The tropics: cradle, museum or casino? A dynamic model for latitudinal gradients of species diversity. Ecology Letters 11, 653-663.
3. Boggs, C. L., Watt, W. B. and Ehrlich, P. R. (2003). Butterflies: ecology and evolution taking flight. University of Chicago Press, Chicago.
4. Brower, A. V. Z. (1996). Parallel race formation and the evolution of mimicry in Heliconius butterflies: a phylogenetic hypotesis from mitochondrial DNA sequences. Evolution 50, 195-221.
5. Burnham, K. P. and D. R. Anderson (2003). Model selection and Multimodel Inference, a Practical Information-Theoretic Approach. Springer, New York, NY.
6. Burns, K.J., Hackett, S.J. and Klein (2002). Phylogenetic relationships and morphological diversity in Darwin's finches and their relatives. Evolution 56, 1240-1252.
7. Dasmahapatra, K. K., Blum, M. J., Aiello, A., Hackwell, S., Davies, N., Bermingham, E. P., and J. Mallet (2002). Inferences from a rapidly moving hybrid zone. Evolution 56, 741-753.
8. Ford, E. B. (1964). Ecological Genetics. The Broadwater press , Welyn Garden City.
9. Grant, P.R. (1999) Ecology and evolution of Darwin's finches. Princeton University Press, Princeton, NJ.
10. Hadfield, J. D. and L. E. B. Kruuk (2010). MCMC methods for mutli-response generalised linear mixed models: The MCMCglmm R package. Journal of Statistical Software 33, 1-22.
11. Hoorn, C., Wesselingh, F. P., Steege, H. ter, Bermudez, M. A., Mora, A., Sevink, J., Sanmartín, I., Sanchez-Meseguer, A., Anderson, C. L., Figueiredo, J. P., Jaramillo, C., Riff, D., Negri, F. R., Hooghiemstra, H., Lundberg, J., Stadler, T. Särkinn, T. and A. Antonelli (2010). Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330, 927-931.
12. Irestedt M., Fjeldsa J., Dalén, L. and Ericson P.G.P. (2009). Convergent evolution, habitat shifts and variable diversification rates in the ovenbirds-woodcreeper family (Furnariidae). BMC Evolutionary Biology 9: 268 doi: 10.1186/147-2148-9-268
13. Jablonski D., Roy, K. and J. W. Valentine (2006). Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient. Science 314, 102-106.
14. Jiggins, C. D., Naisbit, R. E., Coe, R. L. and J. Mallet (2001). Reproductive isolation caused by colour pattern mimicry. Nature,411, 302-305.
15. Kiessling, W. and C. Simpson (2010). On the potential for ocean acidification to be a general cause of ancient reef crises. Global Change Biology 17, 56-67.
16. Losos, J. B., and R. E. Ricklefs. (2009). Adaptation and diversification on
islands. Nature 457, 830-836.
17. Mallet, J., Beltrán, M., Neukirchen, W. and M. Linares (2007). Natural hybridization in heliconiine butterflies: the species boundary as a continuum. Bmc Evolutionary Biology 7, 28.
18. Mittlebach, G. G., Schemske, D. W., Cornell H. V., Allen A. P., Brown, J. M., Bush, M.B., Harrison S. P., Hurlbert A. H., Knowlton, N., Lessios, H. A. McCain, C. M., McCune, A. R., McDade, L. A., McPeek, M. A., Near, T. J., Price, T.D., Ricklefs, R. E., Roy, K., Sax, D. F., Schluter D., Sobel, J.M. and M. Turelli, (2007). Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecology Letters 10, 315-331.
19. Simkin, T, and K. A. Howard (1970) Caldera Collapse in the Galapagos Islands, 1968.
20. Stolarski, J, Kitahara, M. V., Miller, D. J., Cairns, S. D., Mazur, M., Meibom, A. (2011) The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evolutionary Biology (Online) 11, 2-15.
21. Ricklefs, R. E. (2004). A comprehensive framework for global patterns of biodiversity. Ecology Letters 7, 1-15.
22. Ricklefs, R. E. (2007). Estimating diversification rates from phylogenetic information. Trends in Ecology and Evolution 22, 601-610.
23. Ree, R. H. and S. A. Smith (2008). Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57, 4-14.
24. Rull, V. (2011). Neotropical biodiversity: timing and potential drivers. Trends in Ecology and Evolution 26, 508-513.
25. Quental, T. B. and C. R. Marshall (2010). Diversity dynamics: molecular phylogenies need the fossil record. Trends in Ecology and Evolution 25, 434-441.
26. Whittaker, R. J., Willis, K. J. and R. Field (2001). Scale and species richness: towards a general, hierarchical theory of species diversity. Journal of Biogeography 28, 453-470.
27. Wahlberg, N., Leneveu, J., Kodandaramaiah, U., Peña, C., Nylin, S., Freitas, A. V. L., and A. V. Z. Brower (2009). Nymphalid butterflies diversity
following near demise at the Cretaceous/Tertiary boundary. Proceedings of the Royal Society B-Biological Sciences 276, 4295-4302.
28. Wiens, J. J., Graham, C. H. Moen, D. S., Smith, S. A. and T. W. Reeder (2006). Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: treefrog trees unearth the roots of high tropical diversity. American Naturalist 168, 579-596.
29. Alfaro, M. E., Santini, F., Brock C., Alamillo, H. Dornburg, A., Rabosky, D. L., Canevale, G. and Harmon, L. J. (2009). Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proceedings of the National Academy of Sciences 106, 13410-134414.


Group 3:

Araya-Ajoy, Yimen G. (PhD candidate, Max Planck Institute for Ornithology, Germany)
Bendia, Amanda G. (PhD student, IO-USP, Brazil)
Kitahara, Marcelo V. (Post-doc, CEBIMar USP, Brazil)
Lima, Marcos R. (PhD candidate, UnB, Brazil)
Pereira, Noemy S. (PhD candidate, UNICAMP, Brazil)
Shultz, Allison J. (PhD candidate, Harvard University, USA)
Vitonis, João E. V. V. (Masters student, UNICAMP, Brazil)
Wozniak, Natalia J. (Undergraduate student, Adam Mickiewicz University, Poland)

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