Plate tectonic regulation of global marine animal diversity Andrew Zaffosa,1, Seth Finneganb, and Shanan E. Petersa aDepartment of Geoscience, University of Wisconsin–Madison, Madison, WI 53706; and bDepartment of Integrative Biology, University of California, Berkeley, CA 94720 Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved April 13, 2017 (received for review February 13, 2017) Valentine and Moores [Valentine JW, Moores EM (1970) Nature which may be complicated by spatial and temporal inequities in 228:657–659] hypothesized that plate tectonics regulates global the quantity or quality of samples (11–18). Nevertheless, many biodiversity by changing the geographic arrangement of conti- major features in the fossil record of biodiversity are consis- nental crust, but the data required to fully test the hypothesis tently reproducible, although not all have universally accepted were not available. Here, we use a global database of marine explanations. In particular, the reasons for a long Paleozoic animal fossil occurrences and a paleogeographic reconstruction plateau in marine richness and a steady rise in biodiversity dur- model to test the hypothesis that temporal patterns of continen- ing the Late Mesozoic–Cenozoic remain contentious (11, 12, tal fragmentation have impacted global Phanerozoic biodiversity. 14, 19–22). We find a positive correlation between global marine inverte- Here, we explicitly test the plate tectonic regulation hypothesis brate genus richness and an independently derived quantitative articulated by Valentine and Moores (1) by measuring the extent index describing the fragmentation of continental crust during to which the fragmentation of continental crust covaries with supercontinental coalescence–breakup cycles. The observed posi- global genus-level richness among skeletonized marine inverte- tive correlation between global biodiversity and continental frag- brates. To quantify paleogeographic state over time, we devel- mentation is not readily attributable to commonly cited vagaries oped an index that is sensitive to the connectivity of continental of the fossil record, including changing quantities of marine rock crustal blocks, and we apply that index to reconstructed paleo- or time-variable sampling effort. Because many different envi- geographies from an EarthByte (earthbyte.org) paleogeographic ronmental and biotic factors may covary with changes in the rotation model (23). The continental fragmentation index time geographic arrangement of continental crust, it is difficult to iden- series is then compared with estimates of global richness inde- tify a specific causal mechanism. However, cross-correlation indi- pendently compiled from fossil occurrences in the Paleobiology cates that the state of continental fragmentation at a given time Database (paleobiodb.org) (24). is positively correlated with the state of global biodiversity for Global tectonics is also predicted to exert a first-order con- tens of millions of years afterward. There is also evidence to sug- trol on regional patterns of sedimentation (25–28). Therefore, gest that continental fragmentation promotes increasing marine it is conceivable that an observed correlation between fossil richness, but that coalescence alone has only a small negative diversity and tectonics could reflect a sampling bias in fossil or stabilizing effect. Together, these results suggest that conti- data that is related to temporal variation in the abundance nental fragmentation, particularly during the Mesozoic breakup of preserved marine rock (15, 29–33). To assess this alterna- of the supercontinent Pangaea, has exerted a first-order con- tive hypothesis, we also compare our paleogeography and bio- trol on the long-term trajectory of Phanerozoic marine animal diversity time series with an independent time series describ- diversity. ing the amount of North American marine rock (34). Other common data quality concerns in fossil biodiversity studies, paleogeography j paleobiology j biodiversity j biogeography such as incorrect taxonomic assignments (11), should be inde- pendent of paleogeography and are unlikely to drive observed patterns. late tectonics changed the way geoscientists view the dynamic PEarth and its geological history. Among the first to articulate some of the fundamental biological expectations were Valen- Significance tine and Moores (1), who hypothesized that the aggregation of continental crustal blocks into supercontinents may reduce bio- Understanding the processes that govern biodiversity is a cen- diversity and that the breakup and separation of continental tral goal of biology. It has been hypothesized that global blocks may increase biodiversity. Many environmental factors biodiversity is influenced by tectonically driven shifts in the have been cited as potential mechanisms relating biodiversity arrangement of continental crust. We use globally distributed to global tectonics, including changing climate, sea level, nutri- fossil data and quantitative analyses of shifting continen- ent flux, ocean–atmospheric circulation, total habitable area, and tal configurations in paleogeographic reconstructions to test intercontinental connectivity (1–7). Hypothesized biotic drivers this hypothesis. A significant component of the trajectory of of biodiversity may also be tectonically influenced. For exam- marine animal diversity over the past 443 million years is ple, increased nutrient flux from oceanic rifting and continental attributable to the assembly and disassembly of the supercon- denudation could affect global productivity and biodiversity (8), tinent Pangaea. and coevolutionary interactions could be facilitated by changing ECOLOGY geographic connectivity (9). Author contributions: S.F. and S.E.P. designed research; A.Z. performed research; A.Z. Despite the strong theoretical underpinnings of the super- analyzed data; and A.Z., S.F., and S.E.P. wrote the paper. continent coalescence–breakup model of Phanerozoic biodi- The authors declare no conflict of interest. versity (1–7), there have been few quantitative tests of the This article is a PNAS Direct Submission. hypothesis. Most attempts have used biogeographic patterns to Data deposition: The data reported in this paper have been deposited in a GitHub repos- test for evidence of secular trends in provinciality rather than itory (https://github.com/UW-Macrostrat/PNAS 201702297). directly testing for covariation between marine richness and 1To whom correspondence should be addressed. Email: [email protected]. plate tectonics (3, 10). This is, in part, because of concerns This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. EARTH, ATMOSPHERIC, over the accuracy of fossil-based biodiversity reconstructions, 1073/pnas.1702297114/-/DCSupplemental. AND PLANETARY SCIENCES www.pnas.org/cgi/doi/10.1073/pnas.1702297114 PNAS j May 30, 2017 j vol. 114 j no. 22 j 5653–5658 Downloaded by guest on September 30, 2021 Results motions persist, the index will continue to decline as the last rem- Paleogeography. We developed an index to quantitatively nant of the ancient Tethys Sea, the Mediterranean, is eliminated describe the degree of continental fragmentation during the by the collision of Africa with Eurasia. However, opening of the Phanerozoic (Materials and Methods). The index ranges between East African rift may partially offset this decrease. zero and 1, with 1 representing the state in which all continental blocks are completely separated, and zero representing the state Global Biodiversity. Global biodiversity estimates used here in which all continental blocks are contiguous and arranged in a derive from the Paleobiology Database and are broadly compa- way that minimizes their ocean basin-facing perimeter. We cal- rable to other assessments of marine animal richness (12, 14). culate the index only for those continental blocks that are present The specific Phanerozoic trajectory of marine animal genus rich- throughout the entire duration of the Phanerozoic. Together, ness remains contested (11, 13, 15–17, 21), but analyses consis- these persistent continental fragments comprise 88% of total tently reproduce several long-term patterns. A quick rise to a present-day continental area in the EarthByte model (23). volatile Paleozoic plateau (19), a drop during the end-Permian, The continental fragmentation index (Fig. 1) increases at the a prolonged Early Mesozoic recovery, and a subsequent rise (9, start of the Phanerozoic (541 Ma) in response to the breakup and 20–22) that eventually exceeded the Paleozoic maximum in the dispersal of crustal blocks that previously formed the Proterozoic Late Mesozoic or Early Cenozoic (Fig. 2 A and B) are all consis- supercontinent of Rodinia (35). Peak Paleozoic continental dis- tent features of the paleontological literature. assembly occurs at ∼470 Ma, near the Early/Middle Ordovician There are a number of qualitative similarities between the boundary. A series of alternating plateaus and declines follows trajectory of Phanerozoic biodiversity (Fig. 2) and continental the Late Ordovician peak in continental fragmentation, reflect- fragmentation (Fig. 1), which is consistent with the original for- ing the progressive reaggregation of continental blocks, which mulations of the hypothesis (1). These similarities are quanti- ultimately culminated in the formation of the Phanerozoic super- tatively expressed by a positive rank–order correlation between continent Pangaea. continental fragmentation and global