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Sixty-Six Million Years Along the Road of Mammalian Ecomorphological Specialization

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Sixty-Six Million Years Along the Road of Mammalian Ecomorphological Specialization Sixty-six million years along the road of mammalian ecomorphological specialization Borja Figueiridoa,1, Paul Palmqvista, Juan A. Pérez-Clarosa, and Christine M. Janisb aDepartamento de Ecología y Geología, Facultad de Ciencias, Universidad de Málaga, 29071 Málaga, Spain; and bSchool of Earth Sciences, University of Bristol, Bristol BS8 1RJ, United Kingdom Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved May 20, 2019 (received for review December 30, 2018) The fossil record of the large terrestrial mammals of the North qualitative mammalian “Chronofaunas” (20). Here, we investigate American Cenozoic has previously been quantitatively summarized the ecomorphological spectrum of these six evolutionary faunas by in six sequential episodes of faunal associations—“evolutionary fau- analyzing changing patterns in ecomorph (21) diversity, consid- nas”—that correspond well with previously proposed qualitative ering categories of diet, locomotion, and body size. As in our “Chronofaunas.” Here, we investigate the ecological spectrum of previous study, determinations are based on an analysis at genus these faunas by classifying their major taxonomic components into level of those taxa that diversified in synchrony rather than on raw discrete ecomorphological categories of diet, locomotion, and body data of standing generic diversity per time interval. For a given size. To specifically address the potential influence of long-term fauna, this allows the exclusion of those taxa that are asynchronous climatic shifts on the ecomorphological composition of these faunas, or that have very low, or more stable, standing diversities across we analyze via contingency tables and detrended correspondence several time intervals. Accordingly, we classified the genera of the analyses the frequency distribution of ecomorph types within fau- most significant families/subfamilies (i.e., those scoring above 1.0 nas. We show that each evolutionary fauna has a unique, nonran- in each of the evolutionary faunas of ref. 12) into different eco- dom association of ecomorphs, and we identify a long-term trend morphs (Table 1 and SI Appendix, Table S1 and Fig. S1)relatedto toward greater ecomorphological specialization over successive fau- dietary strategies, locomotor modes, and body size classes (22, 23). nas during the past 66 My. Major vegetation shifts induced by cli- These ecomorphological categories follow those in the NOW matic changes appear to underlie the ecomorphological dynamics of (http://www.helsinki.fi/science/now/) database (24). these six temporal associations that summarize Cenozoic North The dietary and locomotor categories of the taxa shown in American mammalian evolutionary history. Table 1 can be broadly ordered in increasing level of ecomor- phological specialization (i.e., toward more restricted niche Cenozoic mammals | Cenozoic climatic change | ecomorphology | breadth) from generalized (presumably more eurytopic) forms to evolutionary faunas more specialized (i.e., presumably more stenotopic) ecomorphs (e.g., in the case of herbivores, from plant-dominated omnivores limatic change and the associated vegetational shift influence with generalized ambulatory locomotion to hypercursorial Cpatterns of faunal dynamics over deep time (1–3). For this grazers; Methods). As in Figueirido et al. (12), we included only large reason, understanding the influence of these changes on the biota terrestrial mammals and performed contingency table analyses is fundamental for modeling future biotic responses to anthro- and detrended correspondence analyses (DCAs) from those pogenically induced climatic and environmental change (4, 5). ecological determinations that characterized the evolutionary The fossil record provides a unique opportunity to understand faunas to specifically address the following questions: (i)Does how the biota has responded to climatic fluctuations and vege- each evolutionary fauna of large terrestrial mammals have a tation shifts over macroevolutionary timescales (6). Terrestrial distinctive nonrandom association of ecomorphs? (ii)Ifso, mammals are an excellent group to use for investigation of the which ecomorphs characterize each of the faunal associations effects of changes in climate and vegetation on biodiversity, as and which define their differences? (iii) Could these long-term they are clearly influenced by such factors today (7) and have an excellent fossil record (8, 9), which affords the opportunity of Significance analyzing patterns of ecological change and biodiversity dy- – namics over deep time (10 12). The six “evolutionary faunas” of large mammal taxonomic di- A number of paleoclimatic proxies show a general overall versity described for the North American Cenozoic have a trend of cooling and increased aridity through the North American nonrandom ecomorphological spectrum and show a long-term Cenozoic (the past 66 My), punctuated by several warmer and – trend toward greater ecological specialization over the past 66 wetter intervals (13 15). This has led to large-scale changes in My. We show here that each successive fauna was character- vegetation over much of the continent consisting of a shift from ized by a change toward more specialized ecotypes; these predominantly tree-covered habitats in the Paleogene to grasslands changes were correlated with vegetation shifts caused by in the Neogene (16, 17). Studies of large mammalian herbivores major climatic changes, which may have promoted the ap- (ungulates: hoofed mammals; here including proboscideans) and pearance of new ecological opportunities and morphological small ones (Glires: rodents and rabbits) document parallel changes innovations. in dietary/locomotor strategies through time (18). Figueirido et al. (12) showed that the generic diversity of large Author contributions: B.F., P.P., and C.M.J. designed research; B.F. and C.M.J. performed terrestrial mammals (primarily families of ungulates and carni- research; J.A.P.-C. contributed new reagents/analytic tools; B.F. analyzed data; and B.F., vorans including large [>1 kg] representatives) of the North P.P., and C.M.J. wrote the paper. American Cenozoic can be quantitatively summarized into six The authors declare no conflict of interest. megaassociations of taxa or “evolutionary faunas” (19). These This article is a PNAS Direct Submission. empirical faunas, which emerged as covarying mammalian clades Published under the PNAS license. in a Q-mode factor analysis, (i) share specific patterns of evolu- 1To whom correspondence may be addressed. Email: [email protected]. tionary dynamics (i.e., times of origination, maximum diversifica- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. tion, and extinction) that correlate with patterns of global climate 1073/pnas.1821825116/-/DCSupplemental. change; and (ii) broadly correspond with the classic North American Published online June 10, 2019. 12698–12703 | PNAS | June 25, 2019 | vol. 116 | no. 26 www.pnas.org/cgi/doi/10.1073/pnas.1821825116 Downloaded by guest on September 26, 2021 Table 1. Analysis of adjusted residuals from contingency tables Evolutionary faunas I II III IV V VI Ecomorphs Pu0-Wa7 To2-Ui3 Wa7-Wh2 Ui3-He2 Wh-Bl He2-RLB Diet Plant-dominated omnivore (Pdo), 50–70% of plant resources 20.462*** 8.049*** −5.887 −6.592 −6.174 −5.030 Folivore–frugivore (Ffr), >50% of fruits and <25% of grass −5.113 8.538*** 16.654*** −3.882 −8.183 −6.535 Browser (Brw), <25% of grass and <50% of fruits −3.236 −7.025 1.725 12.038*** 0.851 −4.831 Mixed-feeder (B-g), 25–75% of grass −5.084 −6.810 −6.239 0.904 6.607*** 7.907*** Grazer (Grz), >75% grasses −4.378 −5.864 −5.373 −6.016 8.156*** 10.684*** Animal-dominated omnivore (Ado), 50–70% of animal resources 5.229*** −5.823 −5.335 2.057* 3.616*** 0.470 Meat (Me), generalized carnivore, 50–70% of meat −1.823 6.731*** 3.641*** −2.983 −1.715 −3.487 † Meat–bone (Meb), hypercarnivore (>70% of flesh) feeding −2.735 0.081 −0.825 2.601*** 3.554*** −3.459 on meat and bone marrow †Meat–insect (Mei), invertebrates and small animal prey −1.337 −1.790 −1.640 −1.837 −2.139 8.075*** Meat-only (Meo), hypercarnivore (>70% of flesh) feeding only −3.282 1.664 −0.961 2.867*** −4.735 3.961*** on meat Locomotion Generalized quadrupeds (Gqu), Generalized quadrupedal 19.628*** 11.357*** −3.409 −12.376 −6.483 −3.884 Subcursorial (Scu), Running forms (low degree) −8.682 3.266** 13.192*** 10.751*** −7.369 −10.614 Cursorial (Cur), Running forms (moderate degree) −5.746 −7.696 −7.068 10.241*** 8.411*** −0.730 † Hypercursorial (Hyp), Running forms (high degree) −6.646 −8.903 −8.176 −6.298 10.151*** 15.865*** †Graviportal (Gra), Very large sized ungulates −2.288 −3.065 7.422*** −2.735 −3.662 4.445*** Body size Body size class 1 (Bs1), <1 kg 19.771*** 5.967*** −3.614 −6.127 −6.952 −4.207 – − − − Body size class 2 (Bs2), 1 5 kg 0.922 5.975*** 2.064* 1.343 2.770 3.929 EARTH, ATMOSPHERIC, Body size class 3 (Bs3), 6–19 kg −4.569 3.922*** 3.340*** 0.098 −0.006 −3.251 AND PLANETARY SCIENCES Body size class 4 (Bs4), 20–89 kg −3.397 −4.889 −2.622 3.279* 5.151*** 0.956 Body size class 5 (Bs5), 90–199 kg −4.675 −4.165 −1.521 3.648*** 2.567** 2.609** Body size class 6 (Bs6), 200–299 kg −2.809 −5.387 −1.337 −1.445 5.091*** 4.384*** Body size class 7 (Bs7), 300–949 kg −2.155 −2.893 3.216** 0.396 −2.687 3.911*** Body size class 8 (Bs8), 950–3,000 kg −2.045 −2.745 3.179** 2.041* −3.273 2.775*** Body size class 9 (Bs9), >3,000 kg −1.293 −1.736 −1.591 −1.774 −2.070 7.819*** Adjusted residuals from the three contingency tables computed for diversity of genera weighted by species classified within each ecomorphological category among the six evolutionary faunas. Separate contingency tables were computed for each category (trophic preferences, locomotion modes, and body size classes).
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