Long-Term Origination Rates Are Reset Only at Mass Extinctions

Downloaded from geology.gsapubs.org on August 18, 2012 Long-term origination rates are reset only at mass extinctions

Andrew Z. Krug and David Jablonski Department of Geophysical Sciences, University of Chicago, 5734 South Ellis Avenue, Chicago, Illinois 60637, USA

ABSTRACT time series of supports for each infl ection point Diversifi cation during recovery intervals is rapid relative to background rates, but the (Fig. 1). The most strongly supported infl ec- impact of recovery dynamics on long-term evolutionary patterns is poorly understood. The tion points stand out as peaks in this spectrum. age distributions for cohorts of marine bivalves show that intrinsic origination rates tend Survivorship curves suffer from two poten- to remain constant, shifting only during intervals of high biotic turnover, particularly mass tial biases that may confound the ability to esti- extinction events. Genera originating in high-turnover intervals have longer stratigraphic mate shifts in origination rates around infl ection durations than genera arising at other intervals, and drive the magnitude of the shift following points. (1) Genus-level BSCs are potentially the Cretaceous–Paleogene (K-Pg) extinction. Species richness and geographic range promote age-dependent, meaning that the elapsed time survivorship and potentially control rates through ecospace utilization, and both richness and since the origination of the genus can alter the range have been observed to expand more rapidly in recovery versus background states. Post- probability that a branching event occurs. If this Paleozoic origination rates, then, are directly tied to recovery dynamics following each mass effect is large, extinction intensity may factor extinction event. into the slopes of BSCs (Foote, 2001), producing infl ection points even when the origination INTRODUCTION resents the net rate of accumulation through rate is constant. (2) Because genus ranges can In the fossil record, mass extinctions are con- time of all genera coexisting at a time win- span multiple stage boundaries, the origination sistently followed by episodes of rapid diver- dow, which makes this method preferable to rates estimated for cohorts are not entirely inde- sifi cation (Erwin, 2001, 2008), but the lasting stage-by-stage rates, which describe origina- pendent. To account for both issues, stage-level impact of these events on evolutionary dynam- tions within a stage but not their contribution per-taxon rates (Foote, 2000) were calculated to ics in the much longer intervals between mass to diversity in future time planes. A constant corroborate rate shifts discussed below. These extinctions is poorly understood. Peaks and val- slope indicates a constant per-taxon origina- origination rates are estimated only from gen- leys in evolutionary rates through time can be tion rate of that cohort (likely underlain by era originating within each stage, so that each interpreted in terms of environmental stresses constancy in the factors governing the origi- estimate is independent of the others. They are inferred from the geological record, but contain nation rate), whereas signifi cant infl ection also independent of the extinction rate within no direct information on the lasting infl uence points in the BSC refl ect prolonged shifts in the stage, eliminating any bias introduced by of those events on faunas in subsequent times. the probability of origination. To identify and age-dependent dynamics. Stages within the Such interval-to-interval variations can occur evaluate the statistical support for potential recovery interval following the end-Cretaceous stochastically even under evolutionary models infl ection points within each BSC over a single (K-Pg) extinction (defi ned here as extending to where the probability of origination or extinc- exponential function, one-parameter (single the Paleocene-Eocene boundary at 55.8 Ma) tion is held constant (Raup et al., 1973; Nee, exponential probability function with slope were excluded from the analysis. See the Data 2006), and may also be infl uenced by variations λ), three-parameter (two exponential functions Repository for analytical details. in sampling and preservation, making it diffi cult separated by an infl ection point tcrit), and fi ve- to identify long-term shifts in evolutionary rates parameter probability functions (three expo- RESULTS and, therefore, the processes that govern them. nential functions separated by two infl ection Additionally, while signifi cant effort has gone points; see the GSA Data Repository1) were fi t Infl ection Points and Shifts in Origination into estimating and interpreting extinction rates, to the data using the optim function in the soft- Rates origination rates have received less attention. ware package R (R Developmental Core Team, For all cohorts from the Early Cretaceous to 2008). The corrected Akaike Information Cri- the Pleistocene, only a few infl ection points and DATA AND METHODS terion was used to determine the best-supported shifts in origination rates were supported (Fig. 1; Here, we analyze the distribution of infl ec- model. Only cohorts containing >100 genera Table DR1 in the Data Repository), consis- tion points within backward survivorship were analyzed to enhance statistical power tently positioned at the same geological events. curves (BSCs; Raup, 1978; Foote, 2001) for in determining infl ection points, limiting the Maximal support for an infl ection point in all a succession of cohorts (defi ned as the set of analysis to cohorts that cross stage boundaries Cenozoic BSCs occurs at the base of the Maas- genera whose stratigraphic ranges cross a between the Pleistocene and the Middle Juras- trichtian (ca. 70.6 Ma); the difference in support stage boundary) of marine bivalve genera—a sic (Aalenian-Bajocian boundary), all together between the base of the Maastrichtian and the well-characterized model system whose tem- spanning ~170 m.y. Every stage boundary K-Pg boundary (ca. 65.5 Ma) is equivocal, and poral and spatial dynamics mirror those of the within the stratigraphic ranges of genera within the slight offset may also refl ect less intense marine biota as a whole (Krug et al., 2009b). the cohort was analyzed (excluding the oldest study in the 75–100 Ma interval, which would BSCs, which plot the number of taxa within 1% of the genera), the rates surrounding the artifi cially concentrate originations in the last a cohort that originated prior to a window of infl ection point determined, and the support 10 m.y. of the Cretaceous (Foote, 2003; Krug observation (Foote, 2001), allow for robust cal- for the model assessed. This analysis yielded a et al., 2009a). Origination rates consistently culations of origination rates and for inferences increase from ~0.015 (Fig. 2A, black points) to into the processes affecting those rates. Assum- 1GSA Data Repository item 2012202, description ~0.032 (gray points) genera/genus/m.y. around ing rates are time-specifi c and taxonomically of data and methods, Tables DR1 and DR2, Figures this infl ection point. Because the infl ection point homogeneous, BSCs defi ne an exponential DR1–DR4, and additional references, is available is consistently at the K-Pg boundary, the recov- online at www.geosociety.org/pubs/ft2012.htm, or probability function whose slope is governed on request from [email protected] or Docu- ery interval is counted toward the Cenozoic by the origination rate of the cohort (Foote, ments Secretary, GSA, P.O. Box 9140, Boulder, CO rate, causing slightly higher estimated Cenozoic 2001). This intrinsic origination rate (λ) rep- 80301, USA. rates for cohorts nearer the Paleocene recovery

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A: Cenozoic cohorts B: Mesozoic cohorts (Fig. 2B), likely representing the recovery interval following the Late Permian mass extinction. Rates for this interval vary due to small sample 3 sizes, and steps in this curve occur with the addi- tion of as few as two genera (e.g., the decrease from 89.3 to 93.5 Ma). Following the recovery 1 2 interval, origination rates decrease into the Tri- assic (0.027) and then again into the Jurassic (0.020; Fig. 2B), coincident with the Late Trias- Proportion of originations Proportion of originations

0.01 0.05 0.2 1.0 0.01 0.05 0.2 1.0 sic mass extinction event. The decrease following the Late Triassic extinction stands in contrast to the increase following the K-Pg extinction. Although Triassic and Jurassic 95% conﬁ dence intervals overlap slightly owing to small sample sizes, the decrease in origination rates is signiﬁ - cant if the Middle Triassic recovery genera (i.e., Support / max Support / max genera that originate within the recovery inter- 1.0 0.99 0.98

1.0 0.996 0.992 val) are excluded and a three-parameter model 0 50 100 150 200 100 150 200 250 is fi t to the data. Time (Ma) Time (Ma) The only infl ection points supported for all cohorts in this analysis occur within one stage Figure 1. Backward survivorship curves (BSCs) (top panels) and support for potential boundary of a mass extinction and/or recov- infl ection points (tcrit) within BSCs (bottom panels) of marine bivalves. A: Cenozoic cohorts. B: Mesozoic cohorts. Support values for bottom panels correspond to stages ery interval. However, other infl ection points within survivorship curves, plotted as the negative of the support returned by the R are statistically supported for smaller groups function optim, so that the lowest values represent the strongest support for an infl ec- of cohorts (Fig. 1; Fig. DR1) and also occur tion point. Support values are normalized to the largest support value for an infl ection point in that cohort. Gray lines represent the support values for individual cohorts, at times of rapid biotic turnover, such as the with thick black line showing the mean for all cohorts at an infl ection point. Thick ver- Berriasian (Kiessling and Aberhan, 2007), the tical dashed lines indicate infl ection points supported for all cohorts between mass Cenomanian (Harries and Little, 1999; Smith extinctions, and are extended to the top panel to highlight the infl ection point within et al., 2001), and the middle Miocene. How- those BSCs. Thin vertical dashed lines represent infl ection points supported for at ever, infl ection points at these boundaries are least three cohorts. Numbers with arrows mark the top boundary of stages with mass extinctions. 1—end-Cretaceous; 2—Late Triassic; 3—Late Permian. not supported for more than three successive cohorts (Fig. DR1). Models incorporating more than two infl ection points begin to lose statisti- A: Cenozoic B: Mesozoic cal power, so rate shifts could only be analyzed around the middle Miocene infl ection point, as only the K-Pg extinction is otherwise supported for Cenozoic cohorts. Here, the data support a drop in origination rates after the infl ection point (Fig. DR2), apparently in conjunction with global refrigeration and the formation of Antarctic glaciers (Zachos et al., 2008), and despite the likelihood of increased sampling in these intervals (Alroy et al., 2008), suggesting a temporary but dramatic role for climatic pre−K-Pg P-Tr recovery Cenoz cooling. However, despite the lasting presence

Origination rate (per genus per m.y.) Origination rate (per genus per m.y.) Tr-J J-K of the icehouse state, the Pliocene–Pleistocene 0.00 0.01 0.02 0.03 0.04 0.05 0.00 0.02 0.04 0.06 0.08 0.10 and Holocene cohorts do not support the mid- 10 20 30 40 80 100 120 140 160 dle Miocene infl ection point, and the Cenozoic Cohort boundary (Ma) Cohort boundary (Ma) origination rate is once again indistinguishable Figure 2. Estimated intrinsic origination rates for cohorts during the Cenozoic (A) and Me- from those estimated from early Neogene and sozoic (B). Each set of points represents the estimated rate for segments of the backward Paleogene cohorts (Fig. DR2). survivorship curve separated by maximally supported infl ection points. Error bars are 95% confi dence interval determined by bootstrap analysis (10,000 repetitions without replace- Stage-Level Per-Taxon Rates Confi rm Rate ment). Error bars for the recovery from the end-Permian extinction (“P-Tr recovery”) in B are excluded for clarity, but are large owing to small numbers and overlap Triassic (Tr) values. Shifts Apparent trend in P-Tr cohort is also an artifact of small numbers (see text). If extinction was producing the infl ection points in BSCs, as could occur if rates were strongly and positively age-dependent (i.e., if interval. This short-lived increase associated Cretaceous and Jurassic cohorts all support older genera within an interval were more likely with postextinction recovery does not bias rate just two infl ection points, the fi rst in the Middle to give rise to new genera), the slopes of BSCs estimates for Paleogene or Neogene cohorts, Triassic (ca. 237 Ma) and the second in the Early would necessarily increase following each and removing the recovery interval does not Jurassic (ca. 196 Ma; Fig. 1B; Table DR1). The infl ection point. The decrease in slope follow- signifi cantly alter the estimated Cenozoic rate highest intrinsic per-taxon origination rates for ing mass extinctions for all Mesozoic cohorts during these times. these cohorts occurred in the Middle Triassic runs counter to this bias. Slopes do increase

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AB C Pectinida Pectinida Pectinida

Anomalodesmata Anomalodesmata Anomalodesmata Carditida Arcida Mytilida Mytilida Mytilida Arcida Arcida Carditida Pteriida Carditida Pteriida Pteriida Lucinida Lucinida Lucinida Nuculanida Nuculanida Myida Nuculanida Myida Myida

Venerida 1 Venerida 1 Venerida 1

Venerida 2 Venerida 2 Venerida 2 Shift in origination rate (per genus per m.y.) −0.01 0.00 0.01 0.02 0.03 −0.01 0.00 0.01 0.02 0.03 −0.01 0.00 0.01 0.02 0.03

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20 Number of recovery genera Number of genera that cross K-Pg boundary Number of long-lived recovery genera Figure 3. Shift in per-taxon origination rates for major bivalve clades following the Cretaceous–Paleogene (K-Pg) mass extinction plotted against (A) the number of recovery genera within each order (Spearman rho = −0.7, p = 0.01), (B) the number of genera that cross the K-Pg boundary (rho = −0.65, p = 0.03), and (C) the number of long-lived genera (rho = −0.8, p = 0.005). All clades were separate by the mid-Meso- zoic, and so are treated as independent points in the Cenozoic. Only genera that ﬁ rst occur in the Danian stage are included in the relevant panels, but the correlation remains signiﬁ cant if genera originating in the Thanetian are included (rho = −0.8, p = 0.003).

following the K-Pg extinction, but stage-level genera (Miller and Foote, 2003). All boundar- infl ection point (Fig. 1), and the stability of the per-taxon rates from the fi ve intervals separated ies showing infl ection points for three or more rates until the next major extinction, make more by infl ection points are perfectly correlated cohorts are within one stage of boundaries with gradual processes unlikely drivers. A second with their BSC estimates (Spearman rho = 1, increases in genus longevity (Fig. 4), except for alternative is that sampling dramatically dis- p = 0.017), confi rming that BSCs are capturing the Albian-Cenomanian boundary (although this places or accentuates infl ection points. How- the average rates. Per-taxon origination rates do infl ection point occurs near a smaller longevity ever, the rapid decrease in support away from vary among stages, but the variation tends to be peak associated with the base of the Aptian) and the maximally supported infl ection points again relatively minor between the infl ection points, middle Miocene (which is too close to the pres- suggests a maximal offset of one stage boundary with 95% confi dence intervals overlapping for ent day to show increased longevity). For K-Pg (e.g., Cenozoic cohorts show similar support for many stages (Fig. DR3). recovery genera, the correlation between the an infl ection point at the K-Pg boundary and the order-level rate shift and the number of long- base of the Maastrichtian; Fig. 1), an error that Recovery Genera Drive Rate Shifts lived recovery genera is stronger (Fig. 3C) than For the Cenozoic, cohorts are suffi ciently the correlation with either all recovery genera or large that the global BSC can be dissected into surviving genera (see Table DR2 for corrected Duration of post-Paleozoic genera major clades (essentially traditional orders; see Akaike Information Criterion values that disfa- AB C D E the Data Repository regarding Venerida 1 and vor more complicated models), suggesting that 2), allowing for a more detailed inspection of newly arising recovery genera set origination the rate shifts at this boundary. The magnitude rates and that the magnitude of the shift is infl u- of the shift in origination rates is unrelated to the enced by the same processes that increase genus extinction intensity for each order at the K-Pg survivorship. boundary (rho = 0.2, p = 0.56; Fig. DR4), indi- cating it is the macroevolutionary or macroeco- DISCUSSION

logical dynamics of recovery, not the severity of The distribution of inﬂ ection points in BSCs Mean duration (m.y.) the bottleneck for each clade, that produces the suggests that changes in intrinsic origina- shift in origination rates. Both surviving genera tion rates occur primarily via the evolutionary

(genera that cross the extinction boundary) and dynamics of mass extinction and postextinction 020406080 new recovery genera appear to be important in recovery. Origination rates do vary from stage to 0 50 100 150 200 250 determining the magnitude of the shift. Order- stage as the biota responds to smaller-scale per- Time (Ma) level rates generally increase following the turbations through time. However, despite these Figure 4. Mean stratigraphic durations of post- K-Pg extinction (Wilcoxon rank sum test, W = fl uctuations, the rate at which each stage contrib- Paleozoic marine bivalve genera originating 97; p = 0.016), and the magnitude of the shift utes to the diversity at a stage boundary remains within each stage. Dashed line represents the is inversely proportional to the number of both effectively constant through time, producing the upper 95% confi dence interval derived from recovery genera (Fig. 3A) and surviving genera log-linear slopes of BSCs (λ) that shift only at a randomization of genus ages within bins. (Fig. 3B) within each order. recovery intervals. Changes in physical condi- Vertical bars mark stages for which bound- λ aries are infl ection points for three or more The lack of signifi cant variation in between tions, including ocean confi gurations (Miller subsequent cohorts. (A—Maastrichtian; B— extinction events may also be attributable to and Foote, 2009), climate state, and/or seawater Cenomanian; C—Berriasian; D—Sinemurian; recovery genera. For post-Paleozoic bivalves, chemistry (Kiessling et al., 2008), might also E—Ladinian.) The middle Miocene infl ection recovery genera have signifi cantly longer strati- promote changes in origination rates during point is marked by an arrow, as this cohort has not had time to accumulate long-lived graphic durations than do genera that originated background intervals, but the abrupt nature of genera. Means are used for comparative pur- in background intervals (Fig. 4), a result con- the rate shifts, as illustrated by the rapid increase poses; statistically more appropriate medi- sistent with previous analyses for all marine in support as the model nears the appropriate ans yield comparable results.

GEOLOGY | August 2012 | www.gsapubs.org 733 Downloaded from geology.gsapubs.org on August 18, 2012 does not bias any rate estimates presented here, valleys so common in the fossil record are never Krug, A.Z., Jablonski, D., and Valentine, J.W., and again, the prolonged stability of background completely divorced from brief, sharp pulses of 2009a, Signature of the end-Cretaceous mass rates in the face of pronounced variation in sam- origination that defi ne recovery intervals. extinction in the modern biota: Science, v. 323, p. 767–771, doi:10.1126/science.1164905. pling and preservation intensity (Foote, 2003; Krug, A.Z., Jablonski, D., Valentine, J.W., and Roy, Sessa et al., 2009) suggests that the fi rst-order ACKNOWLEDGMENTS K., 2009b, Generation of Earth’s fi rst-order patterns discussed here are robust. We thank K. Roy, S.K. Berke, and A. Tomasovych biodiversity pattern: Astrobiology, v. 9, p. 113– for discussions and analytical advice; many bivalve Though the processes that drive shifts in 124, doi:10.1089/ast.2008.0253. systematists for advice and assistance; and M. Foote, Miller, A.I., and Foote, M., 2003, Increased longevi- origination rates are poorly understood, genus J.W. Valentine, and an anonymous reviewer for valu- ties of post-Paleozoic marine genera after mass survivorship has consistently been linked to able comments on the manuscript. This research was extinctions: Science, v. 302, p. 1030–1032, species richness and geographic range, two cor- funded by the NASA Exobiology Program and the doi:10.1126/science.1089719. National Science Foundation. related variables related to the manner in which Miller, A.I., and Foote, M., 2009, Epicontinental seas clades fi ll ecospace. 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