Extinction Selectivity Changes At The Most Extreme Events

A broad array of organismic and clade-level traits enter into extinction risk for present-day species. For example, in evaluating extinction

192 / David Jablonski risk in present-day terrestrial vertebrates, Purvis and colleagues (Purvis et al., 2000b, 2005a; Davies et al., Chapter 14, this volume) found mixed, but significant, effects for body size, a consistent inverse relation between extinction risk and both abundance and geographic range, and either a positive relation or no effect for habitat specialization. Similar patterns are seen in the fossil record. For example, the geographic range is a significant determinant of Cretaceous and Cenozoic molluscan species duration or survivorship [Hunt et al. (2005) and Jablonski and Hunt (2006) and references therein], and Paleozoic crinoids show a significant positive relation between habitat breadth and species duration (Kammer et al., 1998). Predictable interactions among factors can also be seen, although this aspect needs much more work. Molluscan genera containing many widespread species tend to be more extinction-resistant, with a median duration of 130 million years (Myr), than genera having just a few, localized species, which show a median duration of 32 Myr, and the genera with the other combinations give intermediate values (Jablonski, 2005). These are not theoretically surprising results, but it is encouraging that the paleontologi-cal outcomes so clearly match expectations.

Extinction selectivity appears to change significantly at the most severe mass extinctions, however. The rules of survivorship changed during the K-T extinction, such that species-richness and species-level range failed to predict genus survivorship, singly or in concert [Jablonski (1986a, 2005) and see Kiessling and Baron-Szabo (2004) for comparable results for K-T corals]. In fact, survivorship of marine invertebrates in the K-T mass extinction is unrelated to a number of factors that have been shown or hypothesized to be important during more normal times. Besides the two already mentioned, these factors include local abundance, mode of larval development (which is in turn related to fecundity and species-level dispersal capability), estimated generation time, living position relative to the sediment-water interface, and trophic strategy (Jablonski, 2005).

Despite this loss in effectiveness of a variety of organismic, species-and even clade-level traits, survivorship at mass extinction boundaries is not random. Every event seems to show some degree of selectivity, but one factor that seems to have promoted survival for most major groups and most mass extinctions is broad geographic distribution at the clade level (i.e., genera), regardless of species-level geographic ranges. This effect, which has been recorded for many groups and all of the major mass extinctions [see Jablonski (2005) for a tabulation], is again further corroborated in an extensively revised version of Jablonski and Raup's (1995) data on K-T bivalves (Fig. 10.1A and B). This is more than a simple binary effect: bivalve genus extinction is inversely related to geographic range, with strong concordance between the new and old data (Fig. 10.1C). The 70% extinction suffered by the genera found in just one or two biogeographic

A70 60

Victims n=172

1995

1 2 3 4 5 6 7 8 Number of Provinces

1995

1 2 3 4 5 6 7 8 Number of Provinces

1 3 5 7 9 11 13 15 Number of Provinces

1 3 5 7 9 11 13 Number of Provinces

1 3 5 7 9 11 13 Number of Provinces

D 35

neu 20

Rudists

(=pachyodont hinge)

3 5 7 9 11 13 Number of Provinces

FIGURE 10.1 Spatial effects in the end-Cretaceous (K-T) mass extinction for marine bivalve genera. (A, B, and D) Victims of the K-T extinction (A) tended to be significantly less widespread than surviving bivalve genera (B), as measured by the number of biogeographic provinces they occurred in during the Maastrichtian stage just before the event [Mann-Whitney U test, P = 0.00001; new analysis based on an extensive, in-progress revision and update of Jablonski and Raup (1995), omitting rudist bivalves (D) as before, note that their inclusion as narrow-ranging victims would strengthen this result]. Adding provinces to fill gaps in observed geographic ranges strengthens the separation between victims and survivors (75% of victims are unchanged in range size and their median range is unchanged at two provinces; 60% of survivors are unchanged and their median increases from four to five provinces). Some caution is needed, because the proportion of survivors is likely to increase with phylogenetic analysis and further taxonomic standardization of early Cenozoic bivalves, but the major pattern is unlikely to change. (C) Significant inverse relation between extinction intensity and the number of biogeographic provinces occupied by bivalve genera during the K-T extinction (Spearman rank test, P < 0.01). Solid line indicates analysis of revised dataset (n = 289 genera). Broken line indicates analysis of previous version of dataset [Jablonski and Raup (1995); n = 297 genera; 28 genera were added and 36 genera were removed in the revision]. (D) Loss of a major adaptation (the pachyodont hinge) by hitchhiking on geographic distribution. The unique pachyodont hinge structure disappeared with the extinction of these genera at the K-T boundary, signaling the termination of the rudist bivalves (Order Hippuritoida).

194 / David Jablonski provinces is significantly higher than the 20% losses seen for genera found in eight or more provinces [of a global total of 16; following Jablonski and Raup, 1995)]. That said, even 20% represents a major, and highly unusual, drawdown of diversity in this most extinction-resistant part of the biota, equivalent to losing 20% of the most widespread genera in the sea today, such as the mussels (Mytilus, Modiolus) and the scallops (Pecten, Chlamys). [Although not ideal in some respects, analyses were conducted at the provincial scale rather than based on occurrences at individual localities, because clades are distributed not along simple linear coastlines, thereby undermining the use of linear distances or simple latitude/longitude extremes. Binning by province also damps some aspects of sampling and taxonomic uncertainty at the genus level, the range-endpoints of present-day molluscan genera tend to cluster at province boundaries (Campbell and Valentine, 1977; Roy et al., 1996), and the results are robust to different approaches to quantifying province-based range sizes.]

Multifactorial analyses corroborate the importance of clade-level distribution in determining survival during mass extinctions and show the value of testing for interaction among factors. For example, if variables are treated independently in the updated K-T dataset, geographic range remains the most important factor in clade survivorship, but species richness also appears to play a significant role (and body size is insignificant as a survivorship predictor). However, multiple logistic regression models taking the three variables simultaneously into account, using Akaike's Information Criterion (AIC) as a basis for model selection (Burnham and Anderson, 2002), shows species richness to covary with range such that when range is factored out, richness has an insignificant effect on survivorship (P = 0.85, as opposed to P = 0.002 for clade range, in the multiple-factor model). Body size also enters into the multiple-factor model as a weak, but significant, variable, but the multiple-factor model does not have significantly more explanatory power than the geographic range model alone, according both to the similar AIC weights (Table 10.1) and a likelihood ratio test [P = 0.09; see Hosmer and Lemeshow (2000)]. Multi-variate approaches will help clarify patterns of extinction selectivity, even if, as here, they show that survivorship virtually collapses to the single variable of geographic range for K-T bivalves. The overlapping variation in range size among the victims and survivors suggests, however, that additional factors, or strong stochastic elements, enter into the fates of individual clades.

Widespread clades are probably always extinction-resistant compared with narrow-ranging relatives. However, during times of low extinction intensity, range is evidently just one significant feature among many, becoming increasingly important as the crowd of factors influencing taxon duration falls away as intensity mounts. How the relation between range

TABLE 10.1 Testing Models for Bivalve Genus Survivorship During the K-T Mass Extinction

No. of

Models

Parameters

AIC

Weight

P

G** + R + B*

4

347.9

0.58

0.002/0.85/0.03

Geographic range***

2

348.6

0.40

e-6

Species richness***

2

356.2

0.02

0.0001

Body size

2

373.5

e-6

0.94

NOTES: When geographic range (G), species richness (R), and body size (B) are analyzed as independent factors, G is the most important factor, but R is also significant. When the three are analyzed together, R is not a significant factor. Note that the combined model is not significantly better than geographic range alone according to the AIC (for model selection, which essentially weighs the adding of parameters against the improved explanatory power of each model). *P < 0.05; **P < 0.01; ***P < 0.001.

NOTES: When geographic range (G), species richness (R), and body size (B) are analyzed as independent factors, G is the most important factor, but R is also significant. When the three are analyzed together, R is not a significant factor. Note that the combined model is not significantly better than geographic range alone according to the AIC (for model selection, which essentially weighs the adding of parameters against the improved explanatory power of each model). *P < 0.05; **P < 0.01; ***P < 0.001.

and extinction risk varies with extinction intensity is not known and is difficult to assess. The few available data suggest that the relation between extinction probability has a steep slope during times of low extinction intensity, with the most widespread genera suffering negligible extinction at those times (Payne and Finnegan, 2007; Powell, 2007a) (Fig. 10.2A). The simplest view would be that perturbations generally operate at too small a spatial scale to affect these most widespread elements of the global biota. In the major mass extinctions, the y-intercept increases, so that a greater fraction of taxa are lost from all range classes, and the slope probably decreases (Fig. 10.2B). This configuration is much more demanding of the data, so that sparse or noisy data may fail to capture that shallower

FIGURE 10.2 The inverse relation between geographic range and extinction risk appears to vary with severity of extinction. Conceptual model for this variation, such that both slope and intercept may change between times of background (A) and mass extinction (B).

"Background" Extinction

"Background" Extinction

Geographic Range

Mass Extinction

Mass Extinction

Geographic Range

Geographic Range

196 / David Jablonski slope. We know little about whether the slope and intercept change continuously or shift abruptly at thresholds. For obvious reasons, including some very practical ones relating to the present-day biota, this would be good to know.

We also know relatively little about the determinants of geographic range size at the clade level. Organismic traits such as dispersal ability and ecological strategy must play a role, but interactions with biogeographic context, clade history, and many other factors, including the way that clades extend their ranges by speciation across barriers, serve to decouple geographic ranges at the species and clade levels. For example, the geographic ranges of the 213 marine bivalve genera present today at shelf depths on the eastern Pacific margin from Point Barrow, Alaska to Cape Horn, Chile are not significantly related to the median or maximum ranges of their respective constituent species (Jablonski, 2005). Genera can attain broad ranges via a few widespread species, a mosaic of nonoverlapping but narrow-ranging species, or any combination thereof, each apparently equivalent in a mass extinction event (although this equivalence deserves further study). Genus ranges are not simply species attributes writ large, but involve a dynamic that is set at another hierarchical level, by the complexities of speciation, species extinction, and range expansion.

This strong spatial component to extinction selectivity suggests that survival can be determined by features that are not tightly linked to the organismic and species-level traits that are favored, indeed shaped, during times of lower extinction intensities. Even well-established clades or adaptations could be lost simply because they are not associated with those few features that enhance survivorship during unusual, and geologically brief, high-intensity events. As discussed below, the removal of incumbents and the subsequent diversification of formerly marginal taxa are essential elements of the evolutionary dynamic fueled by major extinctions [see also Erwin (2001), Jablonski (2001, 2005), and Erwin, Chapter 9, this volume].

These results also suggest that hitchhiking effects may be mistaken for direct selectivity more often than generally appreciated. Biological traits tend to covary, even across hierarchical levels, and so selection on one feature can drag others along with it, hampering efforts to pinpoint cause and byproduct. Such hitchhiking was detected for bivalve species richness in Table 10.1. Whenever widespread or restricted taxa tend to occupy nonrandom regions of phenotype space, for example in body sizes, trophic habits, or metabolic rates within a major group, hitchhiking becomes a real possibility, an interesting interaction across hierarchical levels where the extinction probabilities of organism-level characters are conditioned by clade-level properties (Jablonski, 2007). For example, the rudist bivalves of the Cretaceous seas (Order Hippuritoida) represent an extreme repat-

terning of the bivalve body plan, with highly modified conical shells and a unique, pachyodont hinge structure (Skelton, 1985; Seilacher, 1998). This clade and its bizarre growth form, including the pachyodont hinge, disappeared in the K-T mass extinction (Steuber et al., 2002), but this loss was probably related less to any disadvantage inherent in the remarkable hinge apparatus than to the restricted ranges of rudist clades (Fig. 10.1D), and perhaps to their reliance in at least some instances on photosymbionts [Seilacher (1998), but see Steuber (2000)], as seen in modern reef-building corals. If the range-frequency distribution of rudists played a role in their demise, with correlated morphologies carried along, then we would expect a similar pattern for the other bivalve orders. This is in fact the case: the five bivalve orders with median genus ranges of one or two provinces suffered significantly more severe K-T bottlenecks (median = 93% genus extinction) than the four orders with median genus ranges of three or more provinces (median = 32% genus extinction; Spearman's rank correlation of median genus range and extinction intensity for orders = 0.74, P = 0.02), as predicted by the hitchhiking argument for rudists. More detailed analyses must await a morphometric or discrete-character study combined with a well-resolved phylogeny of bivalve genera, and these results suggest that such studies would be worthwhile.

The hitchhiking of such striking adaptations on the less flamboyant features that actually determine extinction resistance is probably pervasive, both during background times [hence the large literature on comparative methods and phylogenetic autocorrelation; e.g., Freckleton et al. (2002) and Paradis (2005)] and during mass extinctions. For example, marine bryozoan genera with complex colonies suffer more severely during mass extinctions than simple genera, but colony complexity is also inversely related to genus-level geographic range (Anstey, 1978, 1986), which may well be the ultimate basis for differential survival during the end-Ordovician mass extinction. The end-Ordovician extinction also preferentially removed snails with broad selenizones providing access to the mantle cavity, and planktonic graptolites with multiple stipes creating complex pendant colonies; the K-T extinction also preferentially removed bivalves with schizodont hinges (trigonioids), echinoids with elongate rostra (a clade of holasteroids), cephalopods with complex sutures (ammonites), and a major clade of birds with foot bones that fused from the ankles to the toes (Enantiornithes). All of these losses or severe bottlenecks are more likely to represent correlations, not necessarily with geographic range, but with some other organismic or higher-level factor, rather than direct selectivity on the most striking morphology or functional trait. These extinctions nonetheless truncated or rechanneled evolutionary trajectories through morphospace, and additional examples are plentiful.

198 / David Jablonski

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