Macroevolution of Birds and Mammals

The macroevolution of ecological niches in birds is the core is the core topic of the Emmy Noether research group granted to Dr. Susanne Fritz by the DFG (German Research Foundation). Key external project partners are Prof. Katrin Böhning-Gaese at Senckenberg BiK-F, Dr. Till Töpfer at the Zoological Research Museum Alexander Koenig in Bonn, Dr. Jussi Eronen at the BIOS research unit and University of Helsinki, and Prof Carsten Rahbek at the Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark and University of Copenhagen.

We primarily investigate the evolutionary and ecological processes that shape species` ecological niches. In particular, we study realized climatic niches, i.e. the climatic conditions that living species can be found in, and ecomorphological traits, i.e. the morphological adaptations that enable species to occupy specific ecological niches. The project uses a macroevolutionary comparative framework across selected key taxa of passerine birds with migratory and sedentary species, because migratory and sedentary species experience vastly different climatic conditions throughout the year. Do migratory species track their climatic niches when they move from breeding to wintering areas and vice versa? Is climatic niche evolution across migratory and sedentary birds linked to paleo-climatic conditions? How is climatic niche evolution related to the evolution of ecomorphological traits and to the evolution of migratory behaviour? And can we find a relationship between the speed of climatic niche evolution and the diversification of clades, i.e. the speciation and extinction of avian lineages?

Highlighted publications on macroevolution of birds

Eyres, A., Böhning-Gaese, K. & S. A. Fritz (2017): Quantification of climatic niches in birds: adding the temporal dimension. – Journal of Avian Biology 48: 1517-1531.
An in-depth review of how climatic niches can be quantified from seasonal occurrence data in birds, because many species show seasonal or aseasonal movement behaviours that could mean that they occupy very different climatic conditions through the year. We also present a consistent classification of migratory behaviour for all living 10,443 bird species.

Khaliq, I., Fritz, S. A., Prinzinger, R., Pfenninger, M., Böhning-Gaese, K. & C. Hof (2015): Global variation in thermal physiology of birds and mammals: evidence for phylogenetic niche conservatism only in the tropics. – Journal of Biogeography, 42: 2187-2196.
An evaluation of how much phylogenetic history and the ambient environment experienced by species influence experimentally derived thermal tolerances across birds and mammals. We found that thermal tolerance limits are strongly phylogenetically conserved in tropical species but not in temperate ones.

Jønsson, K.A., Fabre, P.-H., Fritz, S.A., Etienne, R.S., Ricklefs, R.E., Jørgensen, T.B., Fjeldså, J., Rahbek, C., Ericson, P. G. P., Woog, F., Pasquet, E. & M. Irestedt (2012): Ecological and evolutionary determinants for the adaptive radiation of the Madagascan vangas. – Proceedings of the National Academy of Sciences of the United States of America 109: 6620-6624.
A collaboration with colleagues from the Center for Macroecology, Evolution and Climate at the Natural History Museum of Denmark investigating one of the most striking examples of adaptive radiation, i.e. the diversification of a group of species into different ecological niches. The vangas of Madagascar are spectacular because of their incredible diversity in feeding ecology and beak morphology, which we show to be linked to their diversification rates.

Beyond these highlighted publications, Susanne has published on diversification patterns of different passerine bird families, as well as on elevational diversity patterns and the links of functional diversity in frugivorous birds with seed dispersal of their food plants (see her publication list here)

This is the second main topic in the working group of Dr. Susanne Fritz, where we mostly work on large mammals through the Neogene (approximately 23-2 million years ago) until today. Here, we bring together paleontological data on past environmental conditions and extinct species with contemporary data on the current environment and living species. Research in ecology and evolution in general has usually been separate, with paleontological studies investigating extinct taxa through time while neontological studies reconstruct the evolutionary history from molecular phylogenies of only the living taxa. Using large mammals with their excellent fossil record in the Northern Hemisphere as a case study, we address integrative key questions across paleo-ecology and evolutionary biology: Which mechanisms generate spatial and temporal variation in diversity? How do diversity patterns in time and space depend on abiotic drivers such as climate? How do traits evolve, and how is trait evolution influenced by the environment? Which processes determine the temporal dynamics of geographical ranges and ecological niches?

Highlighted publications on fossil and living mammalian diversity

Huang, S., Eronen, J. T., Janis, C. M., Saarinen, J. J., Silvestro, D. & S. A. Fritz (2017). Mammal body size evolution in North America and Europe over 20 Myr: similar trends generated by different processes. – Proceedings of the Royal Society B: Biological Sciences 284: 20162361.
An empirical study applying modern Bayesian statistics to a large Neogene fossil record of ungulates (970 species). We show that the consistent trend of increasing body size over 20 million years was generated through different evolutionary processes in different taxa and regions; for example, large-bodied lineages of even-toed ungulates (Artiodactyla) had higher origination rates, suggesting active selection for larger bodies possibly due to environmental change.

Fritz, S. A., Eronen, J. T., Schnitzler, J., Hof, C., Janis, C. M., Mulch, A. Böhning-Gaese, K. & C. H. Graham (2016): Twenty-million-year relationship between mammalian diversity and primary productivity. – Proceedings of the National Academy of Sciences of the United States of America 113: 10908-10913.
Using fossil records of mammals and plants across North America and Europe, we show that higher primary productivity, i.e. net production of plant biomass, was consistently associated with higher mammalian diversity throughout the Neogene, indicating that this relationship is a general ecological pattern in time and space. However, we also show that present-day patterns do not match the fossil diversity-productivity relationship, suggesting that human activity and Pleistocene climate variability have modified a 20-million-year ecological pattern.

Fritz*, S.A., Schnitzler*, J., Eronen*, J.T., Hof*, C., Böhning-Gaese*, K. & C.H. Graham* (2013): Diversity in time and space: wanted dead and alive. – Trends in Ecology and Evolution 28: 509-516. (* equal contributions)
A conceptual framework for the integration of paleontological and neontological perspectives on fossil and living diversity. We highlight the opportunities arising from capitalizing on data and methods from both disciplines, and show how this integration will advance understanding of the fundamental processes that generate and maintain diversity in time and space.

Turvey, S. T. & S. A. Fritz (2011): The ghosts of mammals past: biological and geographical patterns of global mammalian extinction across the Holocene. – Philosophical Transactions of the Royal Society B: Biological Sciences 366: 2564-2576.
This was a collaboration with Dr. Sam Turvey from the IOZ London which investigated over 200 extinct mammalian species together with present-day extinction risk from the IUCN Red List across all living ~5000 species of mammals. We show high spatial and taxonomic selectivity in Holocene extinctions and present-day risk: during the Holocene (i.e. the last 10,000 years), large-bodied mammals have been more extinction-prone nearly everywhere, but today they are primarily threatened in the tropics. This suggests that human activities cause an extinction filter that has already affected big mammals in Europe, North America and Australia and is now striking across the tropics.

In this third topic studied by the working group of Dr. Susanne Fritz, we use global databases and molecular phylogenies of living species to influences of evolutionary history, species’ traits, and current and past environmental variation on present-day patterns of biodiversity. These regional and global studies often focus on new data or methods, specifically how to include phylogenetic and spatial information or tests of data quality for modern occurrence data. Why are some regions so much more species-rich than others? Why do these hotspots of biodiversity coincide for many groups, but not for others? And what are the underlying evolutionary patterns and ecological processes generating and maintaining the astonishing diversity of Life on Earth?

Highlighted publications on global patterns and processes

Tucker, C. M., Cadotte, M. W., Carvalho, S. B., Davies, T. J., Ferrier, S., Fritz, S. A., Grenyer, R., Helmus, M. R., Jin, L. S., Mooers, A. O., Pavoine, S., Purschke, O., Redding, D. W., Rosauer, D. F., Winter, M. & F. Mazel (2017): A guide to phylogenetic metrics for conservation, community ecology and macroecology. – Biological Reviews 92: 698-715.
An in-depth review of different metrics for phylogenetic diversity, with a guide how to use them to address different research questions. This was the output of an interdisciplinary sDiv workshop [link to: www.idiv.de/sdiv] at the German Centre for Integrative Biodiversity Research iDiv. See also these follow-up papers: Miller et al. 2017 Ecography and Mazel et al. 2016 BioRxiv

Meyer, C., Jetz, W., Guralnick, R. P., Fritz, S. A. & H. Kreft (2016): Range geometry and socio‐economics dominate species‐level biases in occurrence information. – Global Ecology and Biogeography 25: 1181-1193.
An evaluation of the publicly available point occurrence information (>4.5 million points) across global mammals (~5000 species), showing that there are severe species-level biases depending on i) range size and shape, ii) socio-economic conditions (in particular the proximity to research institutes), and iii) ecological species traits that influence detection probability, especially body mass and diurnality. A collaboration with colleagues from the University of Göttingen
Weigelt, P., Kissling, W. D., Kisel, Y., Fritz, S. A., Karger, D. N., Kessler, M., Lehtonen, S., Svenning, J.-C. & H. Kreft (2015): Global patterns and drivers of phylogenetic structure in island floras. – Scientific Reports 5: 12213.
A global study on island floras testing the relative influence of dispersal, environmental filtering, and in-situ speciation on phylogenetic assemblage structure; across nearly 400 islands containing >37,000 plant species, we find contrasting trends in the different major plant groups. Another collaboration with colleagues from the University of Göttingen.

Holt*, B. G., Lessard*, J.-P., Borregaard, M. K., Fritz, S. A., Araújo, M. B., Dimitrov, D., Fabre, P.-H., Graham, C. H., Graves, G. R., Jønsson, K. A., Nogués-Bravo, D., Wang, Z., Whittaker, R. J., Fjeldså, J. & C. Rahbek (2013): An update of Wallace’s zoogeographic regions of the world. – Science 339: 74-78. (* equal contributions)
An update of the global biogeographic regions originally introduced by A. R. Wallace in the 19th century, based on distribution maps and phylogenetic trees of over 20,000 species of terrestrial vertebrates. This was work from Susanne’s postdoc with colleagues from the Center for Macroecology, Evolution and Climate at the University of Copenhagen, and it generated some interesting scientific controversy: comment by Kreft & Jetz 2013 and our response.

Beyond these highlighted publications, Susanne has published on global phylogenetic and biogeographic patterns, including climatic niche conservatism, in mammals and amphibians, as well as the current state and future challenges for macroecology as a field (see her publication list here ). Shan has published on global patterns of parasites and their hosts, as well as on latitudinal gradients and dimensions of diversity in marine bivalves and mammals (see her publication list here).

This fourth topic in the working group of Dr. Susanne Fritz links to the second one, as we study human impacts today as well as from a deep-time perspective. Many species are threatened with extinction today, and the pattern of extinction risk is complex both phylogenetically and geographically. Why are some species and clades more threatened than others? Is it just where they live, so due to spatial variation in anthropogenic threats, or is there something about their biology that makes them more susceptible? Which species traits are commonly associated with high extinction risk from habitat loss, climate change, or overexploitation? Finally, do these trait-extinction risk associations hold across different regions and clades, and can we see the same associations in fossil species that have already gone extinct?

Highlighted publications on human impacts on biodiversity

Tucker, M.A., Böhning-Gaese, K., Fagan, W.F., Fryxell, J.M., Van Moorter, B., Alberts, S.C., … , Fritz, S. A., … & T. Mueller (2018): Moving in the Anthropocene: Global reductions in terrestrial mammalian movements. – Science 359: 466-469.
A multi-author study from the movement ecology group that Susanne contributed to. The study used a unique GPS-tracking database of 803 individual mammals from 57 species and found that in areas with a high human footprint, mammals moved on average only one-half to one-third as much as in areas not impacted by human activity.

Fritz, S. A., Eronen, J. T., Schnitzler, J., Hof, C., Janis, C. M., Mulch, A. Böhning-Gaese, K. & C. H. Graham (2016): Twenty-million-year relationship between mammalian diversity and primary productivity. – Proceedings of the National Academy of Sciences of the United States of America 113: 10908-10913.
Using fossil records of mammals and plants across North America and Europe, we show that higher primary productivity, i.e. net production of plant biomass, was consistently associated with higher mammalian diversity throughout the Neogene, indicating that this relationship is a general ecological pattern in time and space. However, we also show that present-day patterns do not match the fossil diversity-productivity relationship, suggesting that human activity and Pleistocene climate variability have modified a 20-million-year ecological pattern.

Lawes, M. J., Fisher, D. O., Johnson, C. N., Blomberg, S. P., Frank, A. S. K., Fritz, S. A., McCallum, H., VanDerWal, J., Abbott, B. N., Legge, S., Letnic, M., Thomas, C. R., Thurgate, N., Fisher, A., Gordon, I. J. & A. Kutt (2015): Correlates of recent declines of rodents in northern and southern Australia: habitat structure is critical. –PLoS One 10: e0130626. See Fisher et al. below for details.

Fisher, D. O., Johnson, C. N., Lawes, M. J., Fritz, S.A., McCallum, H., Blomberg, S.P., VanDerWal, J., Abbott, B., Frank, A., Legge, S., Letnic, M., Thomas, C.R., Fisher, A., Gordon, I.J. & A. Kutt (2014): The current decline of tropical marsupials in Australia: is history repeating?. – Global Ecology and Biogeography 23: 181-190.
This study and the study by Lawes et al. above were the result of a workshop on ongoing declines of native tropical marsupials and rodents in Australia. Australia has experienced a third of the known historical mammalian extinctions, most of these concentrated in medium-sized species of the arid areas and blamed on introduced red fox. However, since the 1970s dramatic population declines are occurring in small-sized species of the fox-free northern tropics. We found that declining species in the south were medium-sized and in open dry habitats, suggesting continued threat from introduced foxes. In contrast, declining northern species were small and associated with savannah habitats, suggesting an increasing threat from feral cats.

Turvey, S. T. & S. A. Fritz (2011): The ghosts of mammals past: biological and geographical patterns of global mammalian extinction across the Holocene. – Philosophical Transactions of the Royal Society B: Biological Sciences 366: 2564-2576.
This was a collaboration with Dr. Sam Turvey from the IOZ London which investigated over 200 extinct mammalian species together with present-day extinction risk from the IUCN Red List across all living ~5000 species of mammals. We show high spatial and taxonomic selectivity in Holocene extinctions and present-day risk: during the Holocene (i.e. the last 10,000 years), large-bodied mammals have been more extinction-prone nearly everywhere, but today they are primarily threatened in the tropics. This suggests that human activities cause an extinction filter that has already affected big mammals in Europe, North America and Australia and is now striking across the tropics.

Beyond these highlighted publications, Susanne’s PhD with Prof. Andy Purvis at Imperial College London focussed on present-day, global extinction risk in mammals and how this is driven by species’ traits and anthropogenic threats (see her publication list here). Shan has also published on global extinction patterns in mammals (see her publication list here).

Eyres, A., Böhning-Gaese, K. & S. A. Fritz (2017): Quantification of climatic niches in birds: adding the temporal dimension. Journal of Avian Biology 48: 1517-1531, doi: 1111/jav.01308

Huang, S., Eronen, J. T., Janis, C. M., Saarinen, J. J., Silvestro, D. & S. A. Fritz (2017). Mammal body size evolution in North America and Europe over 20 Myr: similar trends generated by different processes. Proceedings of the Royal Society B: Biological Sciences 284: 20162361, doi: 10.1098/rspb.2016.2361

Pearse, W. D., Barbosa, A. M., Fritz, S. A., Keith, S. A., Harmon, L. J., Harte, J., Silvestro, D., Xiao, X. & T. J. Davies (2018). Building up biogeography: pattern to process. Journal of Biogeography 45: 1223-1230, doi: 10.1111/jbi.13242