Sex and the Shifting Biodiversity Dynamics of Marine Animals in Deep Time
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Sex and the shifting biodiversity dynamics of marine animals in deep time Andrew M. Busha,1, Gene Huntb, and Richard K. Bambachb aDepartment of Ecology and Evolutionary Biology and Center for Integrative Geosciences, University of Connecticut, Storrs, CT 06269-3043; and bDepartment of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012 Edited by Michael Foote, University of Chicago, Chicago, IL, and accepted by Editorial Board Member David Jablonski October 6, 2016 (received for review June 30, 2016) The fossil record of marine animals suggests that diversity-dependent (OU-OU), in which diversity approaches and then fluctuates processes exerted strong control on biodiversification: after the around an equilibrium value]. We also tested two-phase models Ordovician Radiation, genus richness did not trend for hundreds of incorporating a shift between simple models. These methods can millions of years. However, diversity subsequently rose dramatically in rigorously identify shifts in the pattern of diversity history that the Cretaceous and Cenozoic (145 million years ago–present), indicat- suggest changes in underlying dynamics. ing that limits on diversification can be overcome by ecological or evolutionary change. Here, we show that the Cretaceous–Cenozoic Fertilization Mechanism radiation was driven by increased diversification in animals that trans- Fertilization mechanisms have never been considered explicitly fer sperm between adults during fertilization, whereas animals that in analyses of marine fossil biodiversity. However, they have broadcast sperm into the water column have not changed significantly been extensively discussed in the case of land plants, with animal ∼ pollination proposed as a key factor in the K-Cz radiation of in richness since the Late Ordovician ( 450 million years ago). We – argue that the former group radiated in part because directed sperm angiosperms (14 18). Pollination of plants by animals, as op- transfer permits smaller population sizes and additional modes of posed to wind, is postulated to permit additional modes of pre- zygotic reproductive isolation, which could enhance speciation in prezygotic isolation, as has been argued previously for the coincident conjunction with other isolation mechanisms (19). This effect radiation of angiosperms. Directed sperm transfer tends to co-occur may be strongest when pollinator and plant species are closely with many ecological traits, such as a predatory lifestyle. Ecological coevolved, limiting gene flow among species, as in orchids (20, specialization likely operated synergistically with mode of fertilization 21). Pollination could also permit increased rarity because un- in driving the diversification that began during the Mesozoic marine common, widely spaced individuals may still reproduce as long as revolution. Plausibly, the ultimate driver of diversification was an in- pollinators are present (18). Interestingly, the greater diversity in crease in food availability, but its effects on the fauna were regulated terrestrial relative to aquatic habitats has also been attributed in by fundamental reproductive and ecological traits. part to differences related to fertilization. For example, motile marine animals do not commonly transmit the gametes of sessile diversity dependence | Phanerozoic | Mesozoic marine revolution | species, as pollinators do on land (22–24). Also, chemical and fertilization | copulation visual signals are transmitted more effectively in air, which could enhance sexual selection and speciation; it could also enable he fossil record provides direct, historical evidence that can animals to find mates at greater distances, which could permit Thelp constrain controls on biodiversification, such as the greater rarity (22, 23). relative roles of diversity-dependent and diversity-independent Significantly, marine species also vary widely in fertilization processes (1–3). Statistical analyses of the well-preserved fossil re- strategy. At a broad scale, these strategies are phylogenetically cord of marine animals support diversity dependence, albeit with a shifting value of equilibrium diversity (4-6, but see refs. 7 and 8 for Significance alternate opinions). Recent analyses suggest that such shifts might be quite substantial: after not trending appreciably for 300 million Fertilization mechanisms explain broad patterns in the taxonomic years (Late Ordovician–Jurassic; ∼458–145 MA), global genus distribution of diversity in marine animals, as argued previously richness approximately doubled in the Cretaceous and Cenozoic (9) for land plants. We argue that fertilization via copulation (or some (Fig. 1A). Here, we probe the fossil record for insights into this other significant interaction among adults) permits additional massive shift in global diversity and present a theory on the un- mechanisms of reproductive isolation and smaller population sizes derlying evolutionary and ecological dynamics. We show that the relative to fertilization via the broadcasting of sperm into the wa- Cretaceous–Cenozoic (K-Cz) radiation was highly selective, with ter, thus enhancing diversification potential. Maximum-likelihood diversity increase concentrated in animals that copulate or other- modeling of paleontological data indicates that the diversity of wise transfer sperm between interacting adults. In contrast, the sperm broadcasters has been limited by diversity-dependent fac- aggregate diversity of animals that broadcast sperm into the water tors for the last 450 million years. In contrast, animals that copu- column has not increased appreciably since the Ordovician. We late, etc., were also limited until the Cretaceous and then radiated argue that directed sperm transfer promoted diversification by dramatically, coincident with apparent major changes in marine permitting additional modes of prezygotic isolation, smaller pop- productivity. Fertilization may have acted synergistically with ulation sizes, and greater ecological specialization. Previous work ecological specialization in promoting diversification, particularly EVOLUTION has cited increased productivity as a driver of the K-Cz radiation in predators. (10–12), but we argue that synergistic interactions between mating strategy and ecology modulated the effects of environmental change Author contributions: A.M.B., G.H., and R.K.B. performed research, analyzed data, and on biodiversification. wrote the paper. To characterize diversity history, we generated sampling-stan- The authors declare no conflict of interest. dardized genus richness curves from the Paleobiology Database This article is a PNAS Direct Submission. M.F. is a Guest Editor invited by the Editorial (PBDB; paleobiodb.org) and used maximum likelihood methods Board. (13) to model diversity history. Models of diversity change include 1To whom correspondence should be addressed. Email: [email protected]. random walk, directional change, and two models that are consis- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. EARTH, ATMOSPHERIC, tent with diversity dependence [stasis and Ornstein-Uhlenbeck 1073/pnas.1610726113/-/DCSupplemental. AND PLANETARY SCIENCES www.pnas.org/cgi/doi/10.1073/pnas.1610726113 PNAS | December 6, 2016 | vol. 113 | no. 49 | 14073–14078 Downloaded by guest on September 27, 2021 conserved in most higher taxa of Metazoa that are abundant as A All Metazoa fossils, so they can be inferred reliably based on taxonomic af- filiation (SI Appendix, Reproductive Faunas). Our first group 1000 (broadcasters) includes animals that broadcast sperm into the water column. Some species broadcast eggs, whereas others re- 800 tain them, but we include both in this group because sperm broadcasting is sufficient to limit interactions during mating. As 600 in wind-pollinated plants, fertilization depends on the vicissi- tudes of transport in a fluid, and fertilization potential decreases dramatically over short distances (25, 26). Thus, individuals often 400 produce copious gametes, and fertilization is enhanced in large, dense populations. Species recognition during reproduction oc- curs only between sperm (or spermatophore) and egg (or mother) (27), and adult–adult interactions are limited to factors such as timing of gamete release. Broadcasting animals include bivalves, brachiopods, bryozoans, cnidarians, sedentary echino- 500 400 300 200 100 0 derms, and several less diverse groups (SI Appendix, Reproductive 600 Faunas). Most broadcasters are nonmotile or not regularly mo- B Nonbroadcasters tile and are suspension feeders, as a sedentary lifestyle precludes 400 many other feeding modes. Most fossil cnidarians are corals, many of which capture small living organisms from the water as food (microcarnivory) and may house photosymbionts. 200 Other animals (nonbroadcasters) transfer sperm directly be- tween adults via copulation or some other interaction (e.g., the s male fertilizing eggs as the female releases them). Whether es 100 fertilization is internal or external, adults must recognize each 80 other and interact directly, and reproductive isolation is driven ichn not just by gametic incompatibility, habitat separation, and the like R 60 but also by behavioral and anatomical barriers at the adult level – 40 (e.g., courtship rituals, physical inability to copulate) (28 32). Behavioral barriers to gene flow and sexual selection are generally Genus believed to facilitate speciation (15, 33–35), and reduced Allee d e 500 400