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Investigating Biotic Interactions in Deep Time University of Vermont ScholarWorks @ UVM College of Arts and Sciences Faculty Publications College of Arts and Sciences 1-1-2021 Investigating Biotic Interactions in Deep Time Danielle Fraser Museé canadien de la nature Laura C. Soul Smithsonian National Museum of Natural History Anikó B. Tóth UNSW Sydney Meghan A. Balk Smithsonian National Museum of Natural History Jussi T. Eronen Helsingin Yliopisto See next page for additional authors Follow this and additional works at: https://scholarworks.uvm.edu/casfac Part of the Climate Commons Recommended Citation Fraser D, Soul LC, Tóth AB, Balk MA, Eronen JT, Pineda-Munoz S, Shupinski AB, Villaseñor A, Barr WA, Behrensmeyer AK, Du A. Investigating Biotic Interactions in Deep Time. Trends in Ecology & Evolution. 2020 Oct 13. This Article is brought to you for free and open access by the College of Arts and Sciences at ScholarWorks @ UVM. It has been accepted for inclusion in College of Arts and Sciences Faculty Publications by an authorized administrator of ScholarWorks @ UVM. For more information, please contact [email protected]. Authors Danielle Fraser, Laura C. Soul, Anikó B. Tóth, Meghan A. Balk, Jussi T. Eronen, Silvia Pineda-Munoz, Alexandria B. Shupinski, Amelia Villaseñor, W. Andrew Barr, Anna K. Behrensmeyer, Andrew Du, J. Tyler Faith, Nicholas J. Gotelli, Gary R. Graves, Advait M. Jukar, Cindy V. Looy, Joshua H. Miller, Richard Potts, and S. Kathleen Lyons This article is available at ScholarWorks @ UVM: https://scholarworks.uvm.edu/casfac/47 Trends in Ecology & Evolution OPEN ACCESS Review Investigating Biotic Interactions in Deep Time Danielle Fraser ,1,2,3,* Laura C. Soul,3 Anikó B. Tóth,4 Meghan A. Balk,3,5 Jussi T. Eronen,6,7,8 Silvia Pineda-Munoz,9 Alexandria B. Shupinski,10 Amelia Villaseñor,11 W. Andrew Barr,3,12 Anna K. Behrensmeyer,3 Andrew Du,13 J. Tyler Faith,14,15 Nicholas J. Gotelli,16 Gary R. Graves,17,18 Advait M. Jukar,3 Cindy V. Looy,19 Joshua H. Miller,20 Richard Potts,21 and S. Kathleen Lyons10 Recent renewed interest in using fossil data to understand how biotic interactions Highlights have shaped the evolution of life is challenging the widely held assumption that Challenging the widespread perspective long-term climate changes are the primary drivers of biodiversity change. New that long-term diversity patterns are approaches go beyond traditional richness and co-occurrence studies to shaped primarily by climate is not possible without using fossil record explicitly model biotic interactions using data on fossil and modern biodiversity. data to understand the role of biotic Important developments in three primary areas of research include analysis of interactions. (i) macroevolutionary rates, (ii) the impacts of and recovery from extinction events, and (iii) how humans (Homo sapiens) affected interactions among non-human Important recent development and application of models that utilize data of species. We present multiple lines of evidence for an important and measurable both living and extinct species have role of biotic interactions in shaping the evolution of communities and lineages enabled analyses to move beyond on long timescales. simply excluding potential abiotic drivers to explicitly modeling biotic drivers for the first time. Biotic Interactions in the Fossil Record Biotic interactions occur when organisms living in the same community directly or indirectly Analyses of paleontological data show fl that biotic interactions shape the in uence one another. Biotic interactions can occur within or among species, be positive or temporal diversity trajectories and negative, and cover a wide range of interactions including predation, commensalism, rates of origination and extinction for mutualism, resource competition, and parasitism [1]. Biotic interactions play an important numerous taxa. role in structuring modern communities (e.g., [2]). Understanding their importance in the past Extinction of keystone species has therefore has the potential to shed light on their role in shaping ancient and recent diversity disproportionate impacts on biotic patterns. Historically, however, the study of biotic interactions in the fossil record has largely interactions among surviving species. focused on direct physical evidence of interactions such as bore holes in shells, plant damage by insects, patterns of bryozoan encrustation, rare occurrences of gut contents, and carnivore Recovery from extinction events can be sped up or slowed down by biotic damage on bones (e.g., [3,4]). Analysis of unusually well-preserved fossil assemblages allows interactions among surviving species. reconstruction of trophic relationships among diverse organisms (e.g., [5]) and earlier work documented long-term trends in ecospace (see Glossary) occupation [6]. However, Historically, humans (Homo sapiens) have acted as large, generalist predators, temporally continuous evidence for biotic interactions (traditionally thought to structure disrupting interaction networks among biodiversity on only very limited spatiotemporal scales [7]) with appropriate temporal resolution non-human species. (i.e., high-resolution stratigraphic sequences) is only rarely preserved. Consequently, paleontologists have focused primarily on the more accessible long-term trends in climate as important regulators of biodiversity and the differential success of species (e.g., [8]); only short-term ecological phenomena or long-term patterns that cannot be explained by climate 1Palaeobiology, Canadian Museum of Nature, Ottawa, ON, Canada have typically been attributed to the outcome of biotic interactions (e.g., [9], but see [6]). 2 fi Biology and Earth Sciences, Carleton However, as the only source of suf ciently long-term data, and in light of several recent University, Ottawa, ON, Canada methodological advances, the fossil record is now uniquely positioned to answer many of the 3Department of Paleobiology and questions at the core of the evolutionary and ecological sciences. Herein, we address Evolution of Terrestrial Ecosystems Program, Smithsonian Institution, important recent advances in understanding the role of biotic interactions in shaping National Museum of Natural History, macroevolutionary and macroecological phenomena in the fossil record (Figure 1) and highlight Washington, DC , USA 4 areas of future research we believe will be illuminating. In this review, we exclude studies of Centre for Ecosystem Science, School of Biological, Earth and Environmental physical evidence for interactions, except where they are used to contextualize large-scale Sciences, UNSW, Sydney, NSW, biodiversity patterns. Australia Trends in Ecology & Evolution, January 2021, Vol. 36, No. 1 https://doi.org/10.1016/j.tree.2020.09.001 61 © 2020 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Trends in Ecology & Evolution Biotic Interactions on Large Spatiotemporal Scales 5BIO5 Institute, University of Arizona, Tucson, AZ, USA Interactions among individuals operate on timescales shorter than the typical temporal 6Ecosystems and Environment resolution of the fossil record (i.e., thousands to millions of years). The effects of biotic Research Programme, Faculty of interactions do not scale up from individuals to species and clades in straightforward ways, Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland but result from a multitude of interactions occurring among large assemblages of individuals, 7Helsinki Institute of Sustainability some of which may have opposing or multiplicative outcomes [7,10]. However, if interspecific Science, Faculty of Biological and and intraspecific interactions impact the ecological and reproductive success of individuals Environmental Sciences, Ecosystems and Environment Research Programme, over large spatiotemporal scales, they can have effects on entire species and clades that University of Helsinki, Helsinki, Finland are measurable on macroevolutionary and macroecological scales (Box 1 and Figure 1) 8BIOS research Unit, Helsinki, Finland 9 [7,11–13]. Such emergent patterns include, but are not limited to, shifts in species Department of Earth and Atmospheric Sciences, Georgia Institute of abundances, diversity, and spatial distributions (e.g., [14–16]), partitioning of trait and Technology, Atlanta, GA, USA phylogenetic space (e.g., [17,18]), change in rates of diversification and morphological 10School of Biological Sciences, change (e.g., [19–23]), and the success or failure of biological invasion (e.g., [20,24,25]). University of Nebraska-Lincoln, Lincoln, NE, USA Although a significant body of theory has been developed to address the cumulative effects 11Department of Anthropology, of biotic interactions (Box 1;[7,11,12,26–29]), empirical tests of models that account for the University of Arkansas, Fayetteville, AR, complexity of paleontological data have lagged behind theory. USA 12Center for the Advanced Study of Human Paleobiology, Department of The development of comprehensive phylogenetic and occurrence-based data sets that include Anthropology, The George Washington extant and extinct species (Table 1) (e.g., [30]) have begun to close this gap by enabling empirical University, Washington, DC, USA 13Department of Anthropology and testing of hypotheses relating biotic interactions to emergent biodiversity patterns (Figure 1). Geography, Colorado State University, Models of evolutionary processes have increased in sophistication to allow explicit
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