BULLETIN OF MARINE SCIENCE. 89(4):877–904. 2013 http://dx.doi.org/10.5343/bms.2012.1083

Dissecting a marine snail species radiation (Conoidea: Turridae: Polystira) over 12 million years in the southwestern Caribbean

Jonathan A Todd and Kenneth G Johnson

Abstract The specialized carnivorous conoidean Polystira comprises the largest marine snail species radiation in the Neotropics with approximately 120 living species known and a rich Neogene fossil record. Here we analyze its patterns of species richness, origination, and extinction over the past 12 My in the southwestern Caribbean (SWC). Taxic analysis of a database comprising 3344 specimens and 114 species shows species richness and sampling intensity to co-vary over this interval. Richness is lowest in the Late Miocene (pre-NN11), then rises and remains approximately constant until the Recent, when it rises sharply. No large peaks in fossil origination rates occur, though extinction rates may increase between 2 and 1 Ma. Well-sampled extinct species had median durations of 0.8–1.75 My, but the large majority of species are rare, confined to one or a few horizons, and have durations of <1 My. Polystira shows the highest species origination rates recorded among marine gastropods (0.585–0.935 My−1), combined with short species durations; 94% of living species evolved within the past 1.6 My. This contrasts with longer durations and slower speciation rates in the hyperdiverse conoidean Conus, but that pattern requires restudy. High post- isthmian diversity—coinciding with increased habitat heterogeneity—contrasts with the massive decline in SWC species richness in another carnivorous gastropod—the “strombinid” Columbellidae. We suggest that diversification of Polystira has been driven by intrinsic feeding-related specialization, whereas regionally the near-extinction of scavenging, non-specialized “strombinids” is a direct response to an extrinsic decline in seasonality and variation in food supply that supports trophic generalism.

Adaptive radiation is thought to be the major process driving large-scale patterns of diversification of life S( impson 1953, Stanley 1979). Our knowledge of this process has increased markedly over the past few decades through the study of extant species radiations. Nevertheless, a better understanding of evolutionary processes would be obtainable through knowledge of the order in which traits evolve, how morphological disparity and ecological traits change throughout the history of a radiation, and the nature of evolutionary trends and their repeatability (Schluter 2000, Wills and Fortey 2000). Though it has become popular to characterize diversification dynamics of species radiations solely from patterns derived from molecular phylogenetic trees of extant representatives, this neontological perspective inevitably underplays the importance of extinction in producing the patterns we see today (Ricklefs 2007, 2009, Purvis 2008, Quental and Marshall 2010). An important reason is that the fossil record reveals that extinction is a ubiquitous and major feature of radiations. Also, it is increasingly clear that even broad aspects of overall diversification dynamics—the interaction of speciation and extinction—can be challenging or impossible to infer solely

Bulletin of Marine Science 877 © 2013 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 878 BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013 from molecular phylogenetic trees of extant species (e.g., Ricklefs 2007, 2009, Rabosky and Lovette 2008, Quental and Marshall 2009, 2010). Our insights into the dynamics of radiation and its relationship to environmental change would undoubtedly benefit from grafting onto the tree those branches removed by extinction from the present day biota. Such branches are potentially retrievable from the fossil record for those organisms with preservable hard parts. From a paleobiological perspective, species occurrence, abundance, and duration metrics are all obtainable from the fossil record and can allow insight into the tempo and mode of speciation events (Cheetham and Jackson 1995, Wagner and Erwin 1995) within a radiation. Despite the extra information that can be obtained by using a tree that is filled out with fossils, there are few studied examples of extant species radiations that have taken advantage of a well-preserved and dense fossil record. Many of the best-studied adaptive radiations concern terrestrial organisms that are not rou- tinely buried in depositional basins and are highly unlikely to be preserved as fos- sils (e.g., Hawaiian Drosophila and silversword alliance, Caribbean Anolis lizards). Other popular taxa comprise aquatic organisms that have skeletons that either have poor potential to fossilize because they are weakly skeletonized or are rou- tinely disarticulated during burial (e.g., cichlid fishes of the African great lakes; Schluter 2000). Aquatic molluscs potentially possess a superb fossil record, but they have been surprisingly under-utilized in studies of species radiation. Perhaps one of the most impressive extant radiations in the marine realm is that of the gas- tropod superfamily Conoidea, a clade of carnivores, whose numerous component radiations are thought to have been driven by feeding specialization (Taylor 1998, Duda et al. 2001, Espiritu et al. 2001, Duda and Kohn 2005). Specialization has been enabled by an extremely rapidly-evolving armoury of peptide toxins that are injected using stabbing radula teeth to immobilize prey (see Olivera 2002, 2006 for summaries). The Conoidea has diversified into an estimated 10,000 described species, comprising >15 families, over the past 65 My (Tucker 2004, Bouchet et al. 2011), with perhaps thousands of collected species yet to be described (Bouchet et al. 2009). One hyperdiverse conoidean clade consists very largely of the well-known cone snail Conus (sensu lato). This clade, family Conidae, has a 55-My history and worldwide includes >720 living species (Appeltans et al. 2012). Unsurprisingly, due to longstanding shell collectors’ interest in Conus, the biology and ecology of its species are better documented than those of any other conoidean. High species diversity has naturally led to examination of its history of diversification. Kohn (1990) used a taxic approach, based on counts of species present or inferred to have been present within time intervals, to interrogate a very large, but admittedly uncritical, database of >2500 records of Conus from the paleontological literature. He assessed changes in species diversity, origination, and extinction rates through geologic time worldwide. To do this, Kohn (1990) placed species in stratigraphic bins, or time intervals, used to amalgamate records of discretely sampled taxa to allow further distributional analysis (see Johnson and McCormick 1999), com- prising coarsely subdivided epochs (e.g., Middle Miocene, Late Miocene). Kohn (1990) concluded that sampled species richness of Conus in the Neogene plum- meted from the Miocene (347 species total) into the Pliocene (152 species total), and then rapidly expanded through the Pleistocene to its all-time high in the todd and johnson: caribbean gastropod species radiation dynamics 879

Recent (then estimated at around 500 species). Intriguingly, this data set indicates that 11% of Miocene, 33% of Pliocene, and 77% of Pleistocene [≤2 Ma] species are still extant. To determine the evolutionary history of Conus in more detail, molecular phylogenetic analyses were made of 138 living species (Duda and Kohn 2005). Rates of sequence divergence were calibrated using closely related species with the oldest fossil records and supposed geminate pairs of species separated by the Isthmus of Panama, the age of vicariance being taken as 3 Ma. The authors concluded that most of the extant species analyzed originated sometime in the Miocene (23.0–5.3 Ma) based on the majority of branching points between lin- eages falling in this epoch (fig. 3 in Duda and Kohn 2005). Based on Kohn’s (1990) analyses, Stanley (2008) further identified Conus as showing an exceptionally high radiation rate among marine molluscs and much higher than those of other conoideans, such as the families Terebridae or Turridae (sensu stricto; the latter as Turrinae in Stanley 2008). This is despite his net diver- sification rate being calculated from extant species diversity and age of the old- est fossils, necessarily it underestimates speciation rates by ignoring extinctions. Stanley interpreted the pattern as a consequence of high trophic specialization due to rapid venom peptide (conotoxin) evolution. However, we now know that (1) rapid rates of evolution of conotoxins may occur across the superfamily as a whole (e.g., Modica and Holford 2010), including the Terebridae and Turridae (sensu stricto) (López-Vera et al. 2004, Holford et al. 2009), and (2) many lineages of extant (and extinct) “non-Conus” conoideans [including Turridae (sensu stric- to)] have spectacular levels of undescribed species diversity (Bouchet et al. 2009, Puillandre et al. 2012). Together, these two points encourage us to re-examine just how exceptional the speciation and diversification rates shown by Conus might be now that we can develop the first set of comparative data from another conoidean. Focal Taxon: Polystira Radiation.—Another highly diverse, but to date undescribed radiation within the superfamily Conoidea, occurs within the fam- ily Turridae (sensu stricto herein; see Bouchet et al. 2011) and is the focus of our study. The genus Polystira has recently been recognized to be highly species-rich with approximately 122 living species (31 studied herein, only three of which have been described) and perhaps several hundreds of extinct species (88 studied here- in, only one of which has been described) that evolved during the past 33 My. Throughout its history, Polystira has been geographically confined to the tropics and subtropics of the Americas (Atlantic and Pacific), where it is the most species- rich marine molluscan radiation yet discovered (J Todd and T Rawlings, Cape Breton University, unpubl data). Until our recent re-examination, the large majority of specimens of extant pu- tative (i.e., undescribed) species (“species” hereafter) had lain misidentified in museum collections under a small number of available specific names, often for decades. In contrast, the fossil species studied herein have largely been collected over just the past 25 yrs by the Panama Paleontology Project (PPP; Collins and Coates 1999; J Todd and T Rawlings, Cape Breton University, unpubl data). For living species, we have studied the tropical western Atlantic (TWA) fauna in most detail and currently (March 2013) recognize 112 Recent species. The WoRMS data compilation (Appletans et al. 2012) lists 15 described Recent species occurring in the western Atlantic (of which we recognize 14 as distinct) and five in the tropical 880 BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013 eastern Pacific TEP( ), all of which we recognize. In contrast, 13 of the TWA spe- cies are recognized by Rosenberg (2009), and 10 of these have been recorded from the Caribbean (see table S6 in Milaslovich et al. 2010). The living TEP fauna has been less well studied, but its described diversity (five) is incomplete with at least five, but possibly more, species remaining to be described. New collections made by the PPP reveal that the extinct TEP Polystira fauna also is inadequately known and requires revision. As a probable adaptive radiation (as contrasted with non-adaptive radiation; see Schluter 2000), the study of Polystira has a number of features to commend it. Firstly, Polystira has proven to be one of the most abundant and frequently occur- ring gastropods in quantitative studies of neotropical marine shelf faunas of the SWC and faunas are particularly well sampled over a period of 12 My from the late Middle Miocene to the Recent (Jackson et al. 1999), enabling the combination of paleontological and neontological information of a well-sampled and diverse species radiation, while obviating any complexities introduced by dispersal and evolution of its species elsewhere. Secondly, despite appearing at first glance to be morphologically very simi- lar (Fig. 1), species of Polystira have moderately morphologically complex shells. These contain the following suites of systematically informative characters at spe- cies and higher systematic levels: (1) protoconch morphology, sculpture, and size; (2) teleoconch size; (3) spiral angle and shape; (4) shape and proportions of spire whorls and shoulder morphology; (5) shape of base of whorl and basal spiral orna- mentation patterns; (6) length, shape, and ornamentation of rostrum; (7) strength,

Figure 1. (Opposite page) Morphological and size disparity across western Atlantic Polystira species. Adult specimens of the 14 described living species, two undescribed living species (B, O) and two undescribed fossil species (M, R) all at the same scale. Apertural and lat- eral views of each specimen except A and J (apertural only). (A) Polystira gruneri (Philippi, 1848), lectotype of Polystira phillipsi Usticke, 1969, AMNH 195454; St. Thomas, US Virgin Islands. (B) Polystira R-GUY-1 Todd; RMNH 81100; off Surinam; 06°32´N, 55°16´W; 37.5 m. (C) Polystira florencae Bartsch, 1934; holotype, USNM 429760; off north coast of Puerto Rico, 18°30´20˝N, 66°22´05˝W–18°30´30˝N, 66°23´05˝W, 33–40 fathoms (60–73 m). (D) Polystira macra Bartsch, 1934; holotype, USNM 430395; off NW coast of Puerto Rico 18°40´30˝N, 64°50´W–18°45´40˝N, 64°48´W; 190–300 fathoms (348–549 m). (E) Polystira sunderlandi Petuch, 1987; holotype, USNM 859896; 50 km south of Apalachicola, Florida, USA (Gulf of Mexico), 29°N, 85°W; 150 m. (F) Polystira starretti Petuch, 2002; HMNS 10143; SSE of Key West, Florida Keys, USA, 114 fathoms (209 m). (G) Polystira bayeri Petuch, 2001; FLMNH 164636 (1 of 12 specs); near Cat Cay, Bimini Islands, The Bahamas, 1–6 fathoms (2–11 m). (H) Polystira jelskii (Crosse, 1865); holotype of Polystira hilli Petuch, 1988, USNM 859949; St James, Barbados, 175–225 m. (I) Polystira albida (Perry, 1811); UMML 30.10633; Martinique; 14°54´N, 61°04´W; 47 m. (J) Polystira formo- sissima (E. A. Smith, 1915); syntype, NHMUK 1915.4.18.309; off Rio de Janeiro, Brazil; 22°56´S, 41°34´W, 40 fathoms (73 m). (K) Polystira antillarum (Crosse, 1865 non d’Orbigny, 1848); MNHN; off Port Louis, Guadeloupe, 130 m. (L) Polystira coltrorum Petuch, 1993; MZUSP 32.708 (1 of 7); off Alcobaça, Espirito Santo Province, Brazil. (M) P. F-GAT-1 Todd; NHMUK GG 22811; Las Lomas, Cativá, Republic of Panama, 9°21.4´N, 79°50.3´W. Gatun Formation, Tortonian, Late Miocene (Las Lomas faunule). (N) Polystira tellea (Dall, 1889); syntype, USNM 93912; Gulf of Mexico, USA; 28.6000°N, 85.5833°W; 111 fathoms (203 m). (O) P. R-FLK-8 Todd; FLMNH 156905, 135 mi SW of Egmont Key, Florida, Gulf of Mexico, USA. 99–101 fathoms (181–185 m). (P) Polystira vibex (Dall, 1889); syntype, USNM 87385 (largest of 3), off Havana, Cuba; 28°N, 82.5°W, 80–127 fathoms (146–232 m).(Q) Polystira lindae Petuch, 1987; holotype, USNM 859895; off Paraguaná Peninsula, Gulf of Venezuela, Venezuela, 12°N, 70°W, 35 m. (R) Polystira F-CAY-16 Todd; NHM local- ity 18734 (=PPP 02237), Punta Piedra Roja, Cayo Agua, Bocas del Toro Province, Republic of Panama, 9°08´31.9˝N, 82°00´32.6˝W. Cayo Agua Formation, Pliocene (Punta Piedra Roja W faunule). todd and johnson: caribbean gastropod species radiation dynamics 881 882 BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013 spacing, and micromorphology of axial ornamentation and its ontogenetic devel- opment; (8) size, strength, profile, spacing, complexity, and micromorphology of primary and subsidiary spiral ornamentation and their ontogenetic development; (9) shape of outer lip and anal sinus and changes through ontogeny; (10) growth patterns, presence, and nature of adult modifications; (11) presence and nature of sexual dimorphism; and (12) shell color patterns. Two major molecular clades are extant—most simply characterized by shell height—one has shells between 10–35 mm tall, the other has shells taller than 35 mm. Indeed, adult shell size is one of the most obvious variables, with height ranging over nearly an order of magnitude within the genus (Fig. 1). Thirdly, species have widely varying ecology; living species in the TWA and TEP occur on a range of dominantly soft, sometimes rubbly, substrates across a depth range of 1–500+ m, and extinct taxa appear to have had a similar ecological range (J Todd and T Rawlings, Cape Breton University, unpubl data). We know little about preferred substrates or habitat specificity though a few species are distinctly eurytopic. Overall, the geographic range of individual species varies from local endemics to widely ranging across either the TWA or TEP, and species vary from rare to abundant. Today, larval development is species-specific and falls into two major groups, non-planktotrophic and planktotrophic as largely inferred from protoconch morphology. Unfortunately, little detailed biology is known for any species. Polystira albida (Perry, 1811) has been shown to possess venom contain- ing a suite of conotoxins; like other conoideans, venom is injected into its prey, presumably to immobilize it (López-Vera et al. 2004). The guts of specimens iden- tified as P. albida, but probably representing a distinct species, contained poly- chaete worms (Leviten 1970) and polychaetes are the prey of at least some other Turridae (sensu stricto) (Heralde et al. 2010). A wide variety of “worms” appear to be the most common prey across the conoidean radiation (Taylor et al. 1993, Olivera 2002). Fourthly, there is the possibility of delimiting extinct species of Polystira that are conceptually equivalent to living “biospecies.” Although there is no a priori reason why well-preserved fossil mollusk species might not correspond in their level of taxonomic inclusiveness to morphologically defined recent species, few studies have been made to demonstrate this (Jablonski 2000). Living Polystira comprises a number of distinct morphological and molecular clades, some containing numer- ous morphologically tightly-structured species (J Todd and T Rawlings unpubl data). However, combined morphological and genetic study reveals what appears to be a one-to-one correspondence between clusters of individuals in gene trees (“biospecies”) and independently assessed shell-based “morphospecies.” However, we have only been able to sample the DNA of about one-fifth (24) of the living spe- cies (sometimes from just one specimen) because the majority of them are known only from empty shells. Use of the same conchological characters for delimitation of extant and extinct species allows us to integrate fossil and Recent species oc- currence data. Undescribed (putative) species have been given taxon labels (sensu Schindel and Miller 2010), e.g., Polystira F-CAY-10 Todd, to function as unique species-level identifiers applied to unpublished species concepts. These will -fa cilitate the linkage of specimens in museum collections, specimen metadata, and data analysis in publications. todd and johnson: caribbean gastropod species radiation dynamics 883

Tectonics and Oceanographic Change in Tropical America.—Tropical America is an ideal geographical arena for examining the role of environmental drivers in generating diversity. A gradual constriction of the seaway(s) extend- ing across the previously submerged Isthmus of Panama led to the present-day Caribbean being cut-off from the East Pacific in the Late Pliocene (Jackson and O’Dea 2013). Changing oceanographic conditions in the SWC led to reduced nu- trient supply, increased habitat heterogeneity and the development of coral reef and associated environments (Todd et al. 2002, Johnson et al. 2007, O’Dea et al. 2007) that were very different from the nutrient-rich upwelling water and typical- ly muddy shelf habitats locally present through the Middle and Late Miocene. This natural experiment in vicariance has also attracted a huge amount of geological and oceanographic attention in the past 30 yrs (reviewed in Coates and Stallard 2013, Jackson and O’Dea 2013). The episodes of major environmental change are now described using a range of proxies with increasing temporal resolution (also Jagadeeshan and O’Dea 2012 and references therein). However, detailed integrat- ed neontological and paleontological research has been possible only through ex- ploiting the record preserved in the large number of Neogene depositional basins, especially those on the TWA margin. These basins preserve extensive suites of shelf sediments often containing exceptionally well-preserved fossils (Jackson et al. 1999: text-fig. 1). Through the work of A Coates and the Panama Paleontological Project and associated studies, the previously poorly-studied sedimentary forma- tions of the SWC are today some of the best characterized and most intensely sampled fossil faunas of the entire Caribbean and the tropics.

Objectives

The SWC is perhaps the paleontologically best sampled and one of the more stratigraphically complete regions within the wide tropical and subtropical dis- tributional range of Polystira. Over the past decade the recent sublittoral fauna of the Panamanian Atlantic coast also has begun to be sampled in detail. Therefore, we have chosen to focus first on the SWC as a contribution to continuing cross- taxonomic studies of faunal change in this region. Using a data set obtained from the integration of Recent Panamanian species occurrences with those from well- documented Neogene deposits from Costa Rica and Panama (see below), we aim to establish the overall patterns of species richness in this region through the last 12 My. In the context of species radiation, we will test whether regional species richness has increased at a constant rate or not. If not, can peaks of origination or extinction, as seen in other studied benthos, be identified and how do they com- pare? In particular, (1) Do peaks in species turnover correspond with the interval of turnover in benthic community composition in the SWC within the Early to mid-Pliocene (ca. 4.25–3.45 Ma; O’Dea et al. 2007, Smith and Jackson 2009)? This is thought to have been triggered by the restriction in movement of Pacific deep water into the Caribbean by a constricting interoceanic strait (Steph et al. 2006). (2) Did a macroevolutionary lag in extinction occur with a peak 1–2 My after the final separation of the Atlantic and Pacific in the Late Pliocene (ca. 3–2.8 Ma; Bartoli et al. 2005)? This pattern has been previously demonstrated in a range of other benthos including reef corals, gastropods, bivalves and free-living bryozo- ans (Jackson and Johnson 2000, O’Dea and Jackson 2009, Klaus et al. 2012). (3) 884 BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013

How do evolutionary patterns in Polystira compare to those of other carnivorous gastropods in tropical America? (4) Considering carnivorous gastropods, is there a decipherable evolutionary signal from considering species diversity change in terms of the interplay of trophic ecology and changing environments? (5) How do species durations and evolutionary rates compare between Conus and Polystira and what does this suggest about the generality of evolutionary patterns within the Conoidea?

Materials and Methods

Collections.—The analyzed data set comprises those Polystira specimens that were complete or well preserved enough to be identified with confidence to species-level. All identifications were made by ATJ . Fossils were obtained from Caribbean-facing geologi- cal basins in Costa Rica (southern Limón Basin) and Panama (Canal Basin and North- west coast of Panama, Bocas del Toro Basin), and within-isthmian basins of the Darién (Chucunaque-Tuira Basin), all of which have recently been re-described and accurately dated (Coates et al. 1992, 2004, 2005, Collins and Coates 1999 and papers therein, McNeill et al. 2000). Sampled horizons range in age from late Middle Miocene-early Late Miocene (11.9–11.3 Ma) to Early-Middle Pleistocene (1.77–0.78 Ma), with a short gap be- tween the Middle Pleistocene and the Recent (Online Table 1). Specimens were obtained from bulk samples and specimen collections (see Jackson et al. 1999), the large majority of which were made by members of the Panama Paleontology Project and deposited in the Naturhistorisches Museum Basel (NMB), Switzerland and the Department of Earth Sciences, Natural History Museum, London (NHMUK). Six collections largely or whol- ly comprising three sections from the Southern Limón Basin (Pueblo Nuevo: Standard Fruit Company, Progressive Baptist Church, and Lomas del Mar: undivided) were collect- ed by HE Vokes and DG Robinson and are deposited in the Department of Paleobiology, Smithsonian National Museum of Natural History (USNM), Washington DC. In total, 2951 fossil specimens representing 88 species (three of which have been described) were identified from 235 collections containing 480 species occurrence records O( nline Table 2). Recent specimens were obtained from dredge samples obtained from along a wide stretch of the Caribbean coast of Panama (fig. 4 in O’Dea et al. 2004). Sampled areas in- clude, from west to east: Bahía Almirante and Bocas del Toro, Golfo de los Mosquitos, Portobelo, and the San Blas Islands. For methods see Johnson et al. (2007). The majority of samples (54 stations) were made by PPP members and are currently stored at the Naos Island Laboratory of the Smithsonian Tropical Research Institute, Republic of Panama. Another 21 stations were represented by specimens housed in the American Museum of Natural History (AMNH), New York; Department of Invertebrate Zoology, Smithsonian National Museum of Natural History (USNM), Washington DC and the Rosenstiel School of Marine & Atmospheric Science (RSMAS), University of Miami collections. In total, 393 recent specimens comprising 26 species were identified from 75 samples containing 103 species occurrence records. (Online Table 2). An additional four species from Caribbean Panama are present in our research collections and these are known only from collections made by shell collectors and dealers. A final species is known from a single museum speci- men from Caribbean Panama (USNM 900692). We consider these five additional species only for analyses of comparative speciation rates among conoidean clades as we lack infor- mation on their abundance. The combined fossil and Recent data were analysed using the R language for statistical analysis and graphics (R Core Team 2013) and may be obtained upon request from the authors. Occurrence Data.—We used a taxic approach for estimating change in spe- cies richness because we lack a phylogeny that includes both living and extinct species. todd and johnson: caribbean gastropod species radiation dynamics 885

Consequently, we could not add ghost ranges and lineages (Norell 1992) to provide a fuller description of species richness through time or to estimate the stratigraphic completeness of our sampling. We used raw occurrence data rather than estimates based on sampling intensity because standard methods of estimating confidence intervals on first and last occurrences of species are based on occurrences rather than presence and absence data (Hayek and Bura 2001, Smith and Jackson 2009). Many Polystira species are known from a few specimens collected from stratigraphically, and evidently chronologically, closely- spaced horizons. Therefore, it is inappropriate to apply confidence intervals to our present analyses taken over broad, 1 My or longer, stratigraphic bins (see below). We consider it unlikely that absence of a species from a time bin subsequent to its last recorded oc- currence is an artefact (cf. Smith and Jackson 2009), supported by the few examples of range-through records where a species is unsampled in a time-bin which lies within its known stratigraphic range (Fig. 2A, Table 1). This indicates the ubiquity of short ranges (see Results) given the wide spread and intensity of the sampling efforts. We reject the alternative interpretation that this pattern reflects poor sampling of rare taxa that may nevertheless have had long, multi-interval durations. Faunules and Stratigraphic Binning.—We compared diversity over time using stratigraphic bins. Our collections and samples typically contain too few specimens to

Figure 2. (A,B) Histogram of (A) Polystira species richness obtained from (B) the number of samples plotted per 1-million-years stratigraphic bin. R = Recent only. Narrow light grey bars in (A) represent range-through species otherwise unsampled from each bin. (C,D) Histogram of (C) Polystira species origination rates (= first occurrences/richness in each 1-million-years bin and the Recent) and (D) extinction rates (= last occurrences/richness in each 1-million-years bin and the Recent). For (A–D) samples were merged into faunules that were then assigned to 1-million-year bins using fractional weighting according to the stratigraphic uncertainty of ages assigned to faunules in which each species first or last occurred. 886 BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013

Table 1. Sampled Polystira species richness, total richness (sampled richness + range-through richness), numbers of first occurrences (FO), last occurrences (LO), origination (O) rate = FO / total richness, and extinction (E) rate = LO / total richness for 1-million-year bins. To calculate FO and LO species were assigned to bins using weighted long-ranges.

Million year bins Sampled richness Total richness FO LO O rate E rate Recent 26 26 24.00 26.000 0.923 . 0.1–1.0 7 7 0.50 7.500 0.071 0.357 1.1–2.0 23 23 7.50 13.000 0.326 0.565 2.1–3.0 30 30 10.00 10.500 0.333 0.350 3.1–4.0 36 37 20.00 18.500 0.541 0.500 4.1–5.0 21 23 7.50 7.000 0.326 0.340 5.1–6.0 28 29 7.25 7.000 0.250 0.241 6.1–7.0 25 26 5.75 5.500 0.221 0.212 7.1–8.0 26 27 7.25 4.500 0.269 0.167 8.1–9.0 38 38 11.25 8.167 0.296 0.215 9.1–10.0 15 15 5.00 4.667 0.333 0.311 10.1–11.0 15 15 5.00 4.667 0.333 0.311 11.1–12.0 3 3 3.00 2.000 1.000 0.667 provide adequate estimates of taxonomic richness or turnover without amalgamating them into larger units and most individual samples are undated. Instead, we used faunules to group fossil collections for analysis and assignation to stratigraphic bins; each of our coarser (uneven) bins contains on average 564 specimens. Faunules are assemblages re- covered from a set of collections from a limited stratigraphic interval and geographic dis- tribution (Jackson et al. 1999). Faunules were defined by the age, location, and lithology of a particular stratigraphic unit. Each faunule is as tightly chronologically constrained as possible, usually based on dates obtained from one or more collections contained within it. Each faunule is assigned an age range based on ages of contained samples. These age ranges include uncertainty of varying length depending on the stratigraphic resolution available. The median uncertainty of faunule ages is 0.9M y. Collections included in each faunule were recovered within a 20 m thickness of stratigraphic section and generally along <1 km, frequently as little as 100 m, of outcrop in maximum linear dimension, though exception- ally up to 1.65 km (Valiente south of Playa Lorenzo faunule) where abundance was low and exposures limited. Faunules include collections taken from a single facies or closely associated facies in a lithostratigraphic formation. Newly made collections of Recent mate- rial made by staff at the Smithsonian Tropical Research Institute were assigned to broad collecting areas but were not assigned to faunules pending further research. Assignment of collections to fossil faunules follows Johnson et al. (2007) and O’Dea and Jackson (2009), but in addition 12 faunules are either new to this analysis or redefined. We analyzed 51 fossil faunules comprising a total of 235 collections (Online Table 2). Two sets of stratigraphic bins were made to dissect temporal patterns of richness and origination and extinction with as much clarity as the precision of dating allowed, these were (1) 1-million-year bins and (2) unequal-interval bins. Stratigraphic ranges of species were calculated as long-ranges (Fig. 3) that extend from the oldest limit of the age assigned to the faunule in which a species first occurred to the youngest limit of the age assigned to the faunule in which a species last occurs (Johnson and McCormick 1999). To determine species richness, species were counted as present in a bin if any part of the faunule age crossed the bin. This approach results in longer estimates of range than the commonly used method of estimated ranges from the midpoints of the age assigned to faunules in which a species first and last occurs. However, this can be justified as observed ranges are always likely to be underestimates of true species durations. todd and johnson: caribbean gastropod species radiation dynamics 887

Figure 3. Two methods used to estimate the duration of a species based on midpoint and long-range age estimates of the faunules containing its first and last occurrences (FO, LO).

(1) Overall, 1-million-year bins contain few faunules with uncertainty in age estimates that do not cross interval boundaries. In other words, many faunules have an age resolution >1 My. As bin length is short relative to the resolution of faunal ages, taxonomic turnover was calculated using the “weighted” method in which first and last occurrences were proportionally allocated to each stratigraphic bin crossed by the age of the faunule in which a taxon first or last occurs (Johnson and McCormick 1999). So, for a species that first occurs in a faunule whose age range starts within a million-year bin, extends through another, and terminates within a third bin, one-third of a first occurrence would be assigned to each 1-million-year bin, irrespective of whether the long range extended wholly or partly across that bin. In the case of imprecisely dated or long-duration faunules­—characteristics of the older faunules in our data set—we prefer this technique as it is conservative and smears first or last occurrences across the range of million-year intervals in which the samples may occur. As such it avoids the generation of spurious peaks and troughs as may result from the commonly used alternative of assigning faunules to million-year bins based on mid-points of stratigraphic date estimates (see discussion in Johnson and McCormick 1999). (2) We also used unequal interval bins to establish broad temporal patterns of richness and to assess adequacy of sampling. Selection of unequal bins was primarily based on: (i) establishing approximately uniform numbers of collections per stratigraphic bin, and (ii) assessing the relative stratigraphic resolution of collections in order to avoid assigning col- lections to narrow time bins in cases of imprecise age estimates (Johnson and McCormick 1999). Our compromise solution was a set of six bins of unequal length with boundaries at 12, 8.3, 5.3, 3.7, 2.7, and 0.1 Ma (the last an arbitrary boundary), and the Recent (Fig. 4A). The first two bins are of Late Miocene age, with their boundary lying at the junc- tion of nannoplankton zones NN10 and NN11. The third bin corresponds to the Early Pliocene (Zanclean stage), the interval during which the major turnover of benthic com- munity composition was focused. The narrow fourth bin is almost equivalent to the Late Pliocene as recently re-defined (= Piacenzian stage); the succeeding Gelasian stage is now considered to belong to the Pleistocene (Gibbard et al. 2010). This bin includes the lower part of calcareous nannoplankton zone NN16 (Berggren et al. 1995) to which a number of collections can be precisely dated (Johnson et al. 2007). The fifth bin approximately corre- sponds with the boundaries of the Pleistocene in its current, extended sense. This interval includes the previously identified peak in last occurrences of those taxa doomed to extinc- tion by changing oceanographic conditions in the newly-isolated Caribbean Sea (O’Dea et al. 2007, O’Dea and Jackson 2009). The final bin represents the Recent, separated by ca. 1 My sampling hiatus from the fossil bins. 888 BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013

Figure 4. (A) Stratigraphic ranges of samples (collections), showing assignment to six un- even length stratigraphic bins with boundaries at 12, 8.3, 5.3, 3.7, 2.7, and 0.1 Ma (arbitrary boundary to separate the Recent) based on the position of their mid-point age. (B) Plot of stratigraphic ranges of 114 Polystira species showing relative precision of range estimates. Midpoint ranges are shown as solid lines and long ranges are shown as dotted lines.

Sampling Completeness.—We assessed the relative sampling completeness within the stratigraphic bins by using cumulative sampling curves produced by calculating spe- cies diversity within pooled samples drawn at random. The plotted curves indicate the median richness from 1000 random sequences. Uneven bins were used to ensure enough samples per bin to compare the shapes of the cumulative curves and to even out as far as possible the numbers of samples across time intervals. todd and johnson: caribbean gastropod species radiation dynamics 889

Results

Species Richness through Time.—We examined how patterns of species richness varied through the 12-My study period by plotting numbers of species and numbers of samples assigned to 1-My stratigraphic bins (Fig. 2A). Overall, change in species richness closely parallels the number of collections (or sam- ples) from which they were obtained (Spearman’s rank correlation: for observed richness ρ = 0.80, P < 0.01; for range-through richness ρ = 0.84, P < 0.001) and suggests that the pattern largely reflects differences in sampling intensity among stratigraphic intervals. There are no strong peaks or drops in species richness independent of sampling patterns. Such a pattern has not been reported in other SWC benthic taxa (e.g., Jackson et al. 1996, Jackson and Johnson 2000, Smith and Jackson 2009) and may suggest that Polystira is not responding simply and directly to environmental changes that strongly influenced regional diversity in other taxa. However, richness in the first two of the well-sampled million-year intervals (11–10, 10–9 Ma), very largely within the Late Miocene, does appear lower in re- lation to sampling intensity than in later intervals. We constructed cumulative sampling plots using the six uneven durations to examine whether the pattern is real or a function of differential sampling intensity (Fig. 5). The curve for the oldest bin (pre-NN10: 12–8.3 Ma) comprises a larger number of specimens than any of the later bins but conversely contains the fewest number of species (17). The curve approaches an asymptote suggesting relatively complete sampling. In contrast, the other curves are much steeper, show similar numbers of species to each other (21–27 species) but also show no hint of leveling off. We conclude that our sampling of the faunules in the Late Miocene (12–8.3 Ma interval) is more complete than that within later intervals and therefore its pattern of apprecia- bly lower diversity cannot be interpreted as a sampling artefact. The faunules in- cluded in this interval are derived from the Gatun Formation (Central Panama) and the Tuira and Chucunaque formations (Darién). Earlier faunal studies have shown that gastropod and bivalve generic diversity is seemingly low in the Gatun Formation compared with many other more recently described SWC formations collected by the PPP, and the same is true for the Darién formations (Jackson et al. 1999, Johnson et al. 2007, Todd unpubl data). We suspect the low diversity of the Gatun Formation is due, in part, to its dominant lithology of fairly monotonous sandy silts deposited over a geographically extensive area, producing low mea- sures of molluscan beta diversity (Johnson et al. 2007: table 2). The massive drop in sampled species richness for the 1–0.1 Ma interval is very likely due to the small number of samples and specimens obtained (Fig. 2B). This is because known sediments of this age have limited exposure in the SWC. The single faunule sampled (Swan Cay faunule) largely represents fore-reef debris, transported downslope (Jackson et al. 1999: appendix 1), is from poorly exposed sediments, and is unlikely to provide an adequate census of regional species diversity in this time interval. The comparatively small number of Recent species in relation to the large num- ber of samples may reflect a drop in richness or a lack of comparability between Recent dredge and fossil bulk samples. We consider that the pattern reflects some aspect of sampling, perhaps a real drop in overall molluscan abundance, rather 890 BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013

Figure 5. Cumulative sampling plots of numbers of specimens within uneven-length stratigraphic bins, indicating relative completeness of sampling and differences in diver- sity. Label next to end-points marked with filled circle. than a drop in richness (see further discussion in Johnson et al. 2007). After the early part of the Late Miocene (NN11+), we consider that regional species richness has remained approximately constant. Overall Patterns of Origination and Extinction.—To examine wheth- er there were peaks in origination or extinction of species we plotted origination rates (= first occurrences/richness) and extinction rates (= last occurrences/rich- ness) by million-year intervals using the weighted approach (Fig. 2C,D, Table 1). Overall, the trend in first occurrences (originations) in our data set is very closely paralleled by the peaks in last occurrences (extinctions). This pattern suggests that sampled originations and extinctions track each other and this helps explain the observation that species richness appears to be more or less invariant. Much of this pattern appears to be driven by the uncertainty in the ages of our samples being greater than the average sampled species durations. The large majority of species (97⁄114, 85%) have mid-point ranges restricted to a single bin of uneven length with only 7% (8⁄114) extending over two and 8% extending over three or four of the bins (Fig. 4B). Many species apparently originate and become extinct within the same stratigraphic bin (Fig. 4B).

A Pliocene Peak in Species Turnover?—There are two peaks in apparent origination, during the Pliocene (4–3 Ma interval) and in the Recent (Fig. 2C,D). The Pliocene peak in originations is matched by a similar, slightly higher, peak in extinctions. These paired peaks occur during a recognized period of pronounced community reorganization (ca. 4.25–3.45 Ma) and it is possible that they reflect high rates of both speciation and extinction as noted for pectinid bivalves (fig. 2A todd and johnson: caribbean gastropod species radiation dynamics 891 in Smith and Jackson 2009). However we consider that it is more likely that our peaks are an artefact produced by the combination of having fairly precise age dates for many of the contained samples (Fig. 4A,B) and greater sampling com- pleteness. This most data-rich million-year interval contains more than twice as many collections as the preceding one (Fig. 2B). Lagged Extinction in the Pleistocene?—Did extinction rates in Polystira rise in the Pleistocene after the post-isthmian uplift collapse in productivity and major reorganization of benthic food web structure (Todd et al. 2002, O’Dea et al. 2007)? To answer this we compared weighted extinction and origination rates in the million-year bins (Table 1) extending from the Late Pliocene into the Pleistocene (3–2 Ma to the 2–1 Ma interval). Although these intervals have iden- tical levels of origination, 0.333 My−1, their extinction levels rise strikingly from 0.350 to 0.565 My−1. The 2–1M a interval has the highest extinction rate of any million-year interval in our data set (Table 1), excluding the earliest bin (12–11 Ma), in which the low richness leads to unstable estimates of rates. This pattern of Pleistocene extinction appears quite distinct from the temporally more extended peak in extinctions seen in cupuladriid bryozoans. The latter starts in the Late Pliocene (at ca. 3 Ma) and is essentially complete before the period of poor sam- pling—common to both data sets—that extends over the last 1 My (figs. 1, 2 in O’Dea and Jackson 2009). Reef corals are the best sampled macrofossil group over the last 1 My and they show a very distinct peak in extinction in the Pleistocene between 2–1 Ma (Klaus et al. 2012). In contrast to the latter we consider it is likely that some, possibly much, of the apparent Pleistocene peak of extinctions in Polystira represents artificially truncated stratigraphic ranges due to poor sam- pling of the Late Pleistocene (1 Ma to Recent interval). This interval has only sev- en species sampled, none of which are range-through records (Fig. 4B, Table 1). This sampling deficit is likely to have pushed back any extinction from the Late Pleistocene interval and artificially heightened the 2–1M a peak, an example of the Signor-Lipps effect S( ignor and Lipps 1982).

Massive Increase in Species Originations in the Past 1.6 Million Years.—In the Recent there are many first occurrences with only two of the 26 sampled species (8%) having a fossil record, Polystira albida (Perry, 1811) and Polystira tellea (Dall, 1889). This percentage drops further if we include five spe- cies known but not sampled from recent Panamanian Atlantic waters (J Todd un- publ data). The lack of sampling from the last million years has, in the case of living species, probably pushed originations forward in the record—the reverse Signor-Lipps effect. Placing all of the Recent first occurrences in the 1–0.1 Ma bin would have emphasized this peak. However, we have chosen to separate them as a distinct “Recent” bin (Fig. 2C) to emphasize the presence of a sampling gap in the Middle and Late Pleistocene. We are confident of the very young age of the extant SWC Polystira fauna because of the intensive sampling that has taken place in the youngest widely exposed and intensively collected strata—the Moin Formation of Early Pleistocene age (Online Tables 2, 3: seven faunules within range 2.2–1.5 Ma) from the Southern Limón Basin. The sample sites there are only 100 km from the Recent sampling area of Bocas del Toro so spatial turnover seems unlikely to have affected these com- parisons. The Moin Formation comprises shallow reefal and peri-reefal sediments 892 BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013 that are highly fossiliferous, containing excellently preserved aragonitic mollusks. Peri-reefal sediments contain abundant Polystira with 16 species, 14 of which (88%) are extinct. We can narrow down the timing of originations by focusing on the youngest three faunules (Cangrejos Creek, Cerro Mocho, and Upper Lomas del Mar Eastern reef tract) that are dated at 1.7–1.5 Ma (Online Table 1). The 102 specimens making up these faunules represent <20% of the total recovered from the Moin Formation (533 specimens) but include 12 of the 16 known species. Ten of these 12 species are now extinct; the only exceptions are again the long-ranging P. albida (mid-point range: 4.25 Ma to Recent) and P. tellea (mid-point range: 3.55 Ma to Recent) (Online Table 3). Judging from this we think it highly likely that almost all (26/28 = 93%) of the Recent sampled Polystira species diversity in the SWC has originated in the past ca. 1.6 My. We were initially sceptical that the Moin Polystira fauna might be composed almost entirely of extinct species given the striking contrast in this respect with the mollusk fauna as a whole. This fauna is the oldest and best sampled “Recent Caribbean fauna” of the SWC with approximately 71% of its prosobranch gastro- pod species still alive today (Robinson 1993). Nevertheless, our detailed morpho- logical comparisons with Recent species across the TWA confirm that the Moin species cannot be interpreted as having migrated away from this region as they are not represented elsewhere in our research data set of 1690 present-day species occurrences and which extends across the entire TWA.

Species Durations and Stratigraphic Precision.—Clearly most living species within the SWC have (truncated) durations of ≤1.7 My. What does the fossil record reveal about extinct species? In particular, how does stratigraphic precision of faunule ages affect our estimation of species durations using long and midpoint ranges? We examined this by comparing the distribution of stratigraphic uncertainty in faunule ages with the distribution of observed stratigraphic ranges for (1) all species—living and extinct, (2) extinct species, and (3) extinct species that occur in more than one faunule. In each case we estimated the stratigraphic ranges of species using both mid-point ranges and long-ranges (Fig. 6). Faunules have a median uncertainty of 0.7 My, ranging essentially from a single time slice (for recent faunules) to a maximum of 3.5 My. Median stratigraphic resolution for fossil faunules is 0.9 My (mean = 1.17 My). The median duration for all species estimated using their faunule mid-point ranges is 0 My (mean = 0.54 My) and the 75th percentile is only 0.47 My, with a maximum duration of 5.95 My. One-fifth (24) of the total of 114 species analysed are restricted to the zero length time-slice of the Recent. These are distorting estimated species durations in the data set because their ranges are truncated in the Recent as they have not yet become ex- tinct. Intriguingly, if we exclude the 26 sampled extant species to minimize range truncation (because the time of extinction of extant species remains indefinite), we find that the median duration of the 90 remaining species remains unaltered, suggesting that much of this signal is due to occurrences restricted to one faunule. However, these data still include extinct singletons with zero-length midpoint ranges, so we removed these to leave just 44 extinct species that occurred in more than one faunule. The estimated range distributions of these remaining species for midpoint ranges (median = 0.8 My, mean = 1.22 My) is almost exactly the same as that of the faunules and confirms that almost all extinct species are restricted todd and johnson: caribbean gastropod species radiation dynamics 893

Figure 6. Box and whisker plots comparing distribution of faunule age uncertainty (n = 59) with the midpoint and long stratigraphic ranges of species. Bars are shown for all sampled species (n = 114), extinct species only (n = 90), and extinct species that occur in multiple faunules (n = 44). For each case, the box indicates the interquartile range, and the whiskers extend to the most extreme data point that is no more than 1.5 times the width of the box. The median is indicated within each box. to a single faunule or multiple faunules with identical age estimates. Therefore, our minimal estimates of range durations (from mid-point ranges) are controlled by the precision of stratigraphic ages assigned to faunules. This result also applies to long-range estimates. We studied the distribution of long taxon ranges in the same three sets; all species, extinct species only, and extinct species with multiple occurrences. All species had a median duration of 1.50 My (mean = 1.67 My) and extinct species had a very similar median value of 1.75 My (mean = 2.06 My). No zero-length ranges are present because all fossil faunules have some uncertainty in their estimated ages. Extinct multiple occurrences give the longest estimate of durations (median = 2.70 My, mean = 2.75 My) but, as before, we may be ar- tificially removing species that genuinely are rare so that they are unlikely to be recovered without extremely intensive sampling. Such taxa might be likely to have short stratigraphic durations as ecological theory would predict increased prob- ability of extinction for rare species (Gaston 1994). For the one-half of the extinct species (44⁄90) that probably contain the best sampled, we consider that a conser- vative (i.e., biased upwards) estimate of average species durations may be derived from median values of extinct species with multiple occurrences. Our estimate lies between 0.80 and 1.75 My using mid-point and long-ranges. This leaves about one-half of the species restricted to a single faunule, of these many but not all have 894 BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013 been recovered much too rarely for us to be able to estimate ranges. Frequently occurring single-faunule species will require techniques other than binning to measure their stratigraphic ranges. It is notable that the two species with the longest ranges, Polystira F-CAY-12 Todd (long-range = 5.95 My) and P. F-MOI-3 Todd (long-range = 5.30 My) both have long stratigraphic sampling gaps between their oldest record and the much younger unit containing the large majority of their records. In each case doubt arises due to specimen incompleteness as to whether the taxon-concept truly represents a single species: we think it likely that it does not. Polystira albida has the longest mid-point range (4.25 My) of any confidently identified species in our data set. When Did the Oldest Living Species Evolve?—It may not be a coincidence that the oldest living Polystira (P. albida, 4.25 My) is of very similar age to the oldest (ca. 4.5 My) of the 22 pectinid species alive today in the SWC (Smith and Jackson 2009: appendix 1). Both first occur in the study region during the period in which local oceanographic conditions may have first approximated those of today. These conditions include an absence of upwelling and a concomitant re- duction in nutrient supply (as determined by the MART proxy, an estimate of mean annual range of temperature derived from bryozoan zooid sizes: O’Dea and Okamura 2000), and the presence of carbonate-rich habitats that are locally coral-dominated (O’Dea et al. 2007). In contrast, seven of the 13 most common living species of cupuladriid bryozoans in the SWC with a good fossil record have mid-point ranges >7 My (O’Dea and Jackson 2009: fig. 1). Although these species evolved in different environmental conditions to those in which they thrive today, they were able to adapt their life history strategies and persist.

Discussion

Comparative Species Durations and Speciation Rates.—Extant species of Conus, if we take the results of Kohn’s (1990: fig. 2) analyses at face value, tend to have much longer species durations than extant Polystira, with 7.6% of living Conus species having recorded durations >5.3 My (Pliocene to Recent) (cf. 0% Polystira) and 10% with durations >2 My (cf. 7.6% Polystira). However, these values should be regarded as rough approximations. The short durations of living Conus species were explained by Kohn (1990) as resulting from overall high extinction and subsequent origination rates in the Plio-Pleistocene, though low diversity in the Pliocene was later reassessed as more likely due to relatively poorer fossil re- covery from this interval (Duda and Kohn 2005). Our estimates of species origination rates in Polystira using 1-million-year stratigraphic bins, and excluding poorly sampled intervals, range from 0.221 to 0.541 My−1. As much as 94% of extant species do not occur in the fossil faunules, suggesting an even higher origination rate in the past 1 My (Table 1). In com- parison, during the most rapid period of diversification of Conus, over the past 2 My (late Early Pleistocene–Recent), species origination rate was 0.405 My−1 (Kohn 1990: figs 2, 3: using estimated Recent diversity as 500 species with 95 of these present at 2 Ma). Molecular phylogenetic study of Conus from the Cape Verde Islands (Cunha et al. 2005) reveals that the “small-shelled clade” has evolved at least 32 extant species within the last ca. 3.8 My (derived from fig. 5 in Cunha et todd and johnson: caribbean gastropod species radiation dynamics 895 al. 2005) estimating a speciation rate of 0.263 My−1 using the same taxic approach. Within Polystira such rates of speciation are not at all exceptional—both lie within the range of rates estimated from a well-sampled 1-million-year interval to the next (Fig. 2B, Table 1). The maximal origination rate in Polystira can be judged as lying between a figure more than double the faster of the two Conus rates, 0.935 My−1 (assuming 29 of 31 known Recent species evolved in the last 1 My), and a more modest 0.585 My−1 (assuming the origination interval to be 1.6 My). Though the diversification in the Cape Verde Islands has been described as an “explosive radiation” (Duda and Rolan 2005) it does not seem to match the speciation rates of Polystira lying outside an island radiation setting. Is Polystira an Exceptional Turrid?—With a current estimate of 120 living species, Polystira comprises the largest species radiation in any tropical American marine gastropod genus (J Todd and T Rawlings unpubl data). However, the de- gree to which its rates of speciation are truly exceptional among conoideans in this or any other region has not been studied despite the intense neurobiological and pharmacological interest in the conoideans (Olivera 2006). The living diver- sity of most genera of Turridae (sensu stricto) other than Polystira is concentrated in the Indo-West-Pacific IWP( ). Here recent work delimiting and describing newly collected material has revealed high levels of previously uncollected or unrecog- nized species diversity (e.g., Olivera 2004, Kilburn et al. 2012, Puillandre et al. 2012). Preliminary molecular phylogenetic analyses have placed Polystira as the sister clade to the rest of the living Turridae (sensu stricto; Puillandre et al. 2011a). Determining whether Polystira has speciated more quickly than other species- rich genera of Turridae (sensu stricto) in the IWP, or elsewhere throughout the ca. 67-My stratigraphic range of the family (Tucker 2004), will require far more integrated systematic studies of clades with both fossil and living representatives. Are There General Patterns of Diversification in the Conoidea?— For Conus one might interpret the pattern of diversification writ large as being due to variably low to high levels of origination combined with long species durations. In contrast Polystira shows extremely high levels of origination combined with very short species durations. But how real are these apparent differences? Before looking for an explanation we must assess the accuracy of the patterns from which these characterizations are drawn. Our integrated systematic treatments of fossil and Recent specimens of Polystira based on a combination of relatively complex shell morphology and molecular genetics give us confidence in our species (=taxon) concepts. Our estimates of du- rations have been derived from the continuing stratigraphic work on the isthmian deposits using a combination of biozonations, and magnetostratigraphic and ra- diometric dating. This situation contrasts with that for Conus in four major respects: (1) there is growing interest in discriminating living species of Conus using molecu- lar techniques. These studies are revealing an increasing number of seemingly conchologically finely delimitable but separable species, though some genuinely conchologically cryptic species also seem to be present (Duda et al. 2008, 2009). Consequently estimates of living diversity based on currently known material are increasing and some species with unclear taxonomic status using traditional shell characters have been confirmed as distinct (Duda et al. 2008, Puillandre et al. 896 BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013

2011b). (2) The taxonomy of the fossil occurrence records of living species mostly have not been critically assessed (Kohn 1990, Duda and Kohn 2005) or updated since they were published, sometimes a century ago. (3) An unknown, but perhaps significant, proportion of the fossil occurrence records in Kohn’s database con- tain original, but now outdated, stratigraphic information. Use of this will lead to the derivation of inaccurate absolute dates for fossil calibration in molecular phylogenetic analyses. It is possible that the supposed Pliocene worldwide decline in diversity shown by Kohn’s 1990 analysis may be due in part to strata of this age being considered of Miocene age in the original publications (J Hendricks, San José State University, pers comm). (4) Cone snails have relatively character-poor shells and many closely related species are separated on color patterns and small proportional differences in shell measurements R( öckel et al. 1995). Although we think these fine-scaled characters may be available equally in well-preserved fos- sils, we suspect that fossil Conus specimens have rarely been examined in the degree of detail required to delimit fossil equivalents of narrowly separable liv- ing biospecies. It seems likely that a combination of all four of these points has led to a general over-estimation of Conus species durations and under-estima- tion of speciation rates. This may help us understand the discordance between the exceptionally high species diversity and supposedly long species durations of Conus, with speciation rates that seem to have been rapid only in the past few mil- lion years but to have been much slower during its previous long geologic history (Kohn 1990). If our inference is correct then it is possible that the fairly rapid spe- ciation rates shown by Conus during the last few million years are perhaps typical of rates through geologic time rather than being unusual (see Duda et al. 2008). The plausibility of this interpretation is shown by a parallel case in Polystira. Detailed morphological study of the P. albida clade, a group of large, conspicu- ous, and morphologically very similar species, reveals that P. albida itself ranges back only to the Early Pliocene (ca. 4.25–5.3 Ma), when other closely related but extinct species of the same clade also existed (J Todd and U Smith unpubl data). If we examine the literature record of this species we find that its published geo- logical range extends from the Early Miocene (23.03–15.97 Ma) to the top of the Early Pleistocene (0.78 Ma; data within the Paleobiology Database: http://paleodb. org; accessed 16 October, 2012). At least 10 My of this species’ supposed history is therefore spurious and comprised of specimens that require re-identification. Post-isthmian Fates of Caribbean Carnivorous Snails.—There are a number of suitable candidates for detailed studies of diversity change within a trophic framework in our SWC collections but the necessary species- or subclade- level studies, particularly of species-rich clades, are time consuming and require conchological expertise. So far few have been made. One taxonomic group that has been extensively systematized (though not entirely, given the extensive collec- tions from Bocas del Toro made since Jung’s 1989 monograph) is the “Strombina group” of the Columbellidae. This group shows a very different pattern of chang- ing species diversity through time. A massive extinction in “strombinid” gastro- pods occurred throughout the TWA in the Late Pliocene (extinction rate = 0.50 My−1) and Pleistocene (figs. 9.2, 9.3 in Jackson et al. 1996). Including just three living species, the current TWA fauna is highly depauperate compared to its early Pliocene peak of 27 recorded species, and contrasts strongly with its high extant todd and johnson: caribbean gastropod species radiation dynamics 897 diversity in the TEP (33 species; Jackson et al. 1996). The life habits of “strombi- nids” are not well studied but at least some species primarily seem to be scavengers (Fortunato 2003) and below we will argue that this trophic trait offers a possible explanation for this group’s demise in the TWA. For all marine gastropods known to scavenge, this habit is facultative and is focused in those carnivorous taxa with generalist diets (Britton and Morton 1994). Although there are no compiled data for the relative extinction vs origination rates for species for other clades of scav- engers, some other data suggest this trophic group may have declined in diversity in the SWC post-isthmian seaway closure. The best documented and most-species rich group containing scavengers is the family Buccinidae (now known to include Nassariidae). Scavenging is a principal feeding habit among the buccinids, many of which are generalized carnivores (Britton and Morton 1994). Cross-isthmian comparisons of sessile benthic community development on settling plates have been made by Birkeland (1987). On hard substrates at least, in comparing up- welling regions of the TEP (e.g., Gulf of Panama) to the neighboring oligotrophic Caribbean, there is a marked increase in numbers of smaller, rapidly growing het- erotrophic animals that buccinids prey upon and that show high turnover in re- sponse to pulses of nutrient upwelling. From a theoretical perspective, Valentine (1983) has hypothesized that in highly seasonal environments trophic generalism (i.e., generalist predation and scavenging) is expected to emerge as an adaptive strategy in shelf invertebrates. Turning this on its head we predict that abun- dance (both relative abundance and biomass) and taxic diversity of other unspe- cialized carnivores and facultative predators, in addition to “strombinids,” will have dropped in the Caribbean as a response to its post-closure oligotrophication. A large relative decline (50%) in generic diversity of buccinids surviving in the so-called Gatunian province post-closure (Vermeij and Petuch 1986) may provide some support for this prediction but detailed re-examination of this using the much better sampled collections now available is necessary. Conversely, in the TEP “strombinid” diversity almost doubled (19 to 33 species) in the post-isthmian uplift Pleistocene (figs. 9.2, 9.3 in Jackson et al. 1996). This pattern would be that predicted as a result of a considerable increase in nutrient supply in the TEP due to isthmian closure: modeling experiments suggest that just this occurred (Schneider and Schmittner 2006) as does the alkenone record—a proxy for phytoplankton productivity—in ODP core 846 from the TEP (Lawrence et al. 2006). At present our study of fossil and recent Polystira species diversity in the TEP is too preliminary to compare to the results available for the “strombi- nids” or pectinids (Smith and Jackson 2009). The contrast in fortunes of the “strombinids” and ofPolystira in the SWC post- closure is striking. In contrast to a generalized carnivory and scavenging habit of the “strombinids,” almost all studied conoideans are specialized predators. Indications from experimental work on three species of the confamilial genera Gemmula and Lophiotoma [Gemmula diomedea Powell, 1964, Gemmula speciosa (Reeve, 1842), and Lophiotoma acuta (Perry, 1811)] are that they specialize on ter- ebellid polychaete prey (Heralde et al. 2010). Gut content analyses of specimens of a Polystira species, distinct from but closely related to P. albida (Leviten 1970, J Todd unpubl data), revealed unidentified polychaete remains. Polystira occurs predominantly on soft bottoms, and at least part of one TWA clade with Panamanian species is apparently confined to shallow sea grass 898 BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013 meadows (J Todd and T Rawlings unpubl data). It seems likely that an increase in shallow water habitat heterogeneity, including reef development, was associ- ated with increasing physical and environmental complexity across the isthmian archipelago during seaway closure (Todd et al. 2002, Johnson et al. 2007, O’Dea et al. 2007, Jagadeeshan and O’Dea 2012). This would have subdivided populations of Polystira (along with all benthos) leading to increased species diversity in this small region relative to other areas of the Caribbean today. We intend to examine cross-Caribbean diversity patterns of living species of the genus to see if the high diversity in Panama is a general or more localized pattern across its distributional range. In particular, examination of whether changes have occurred in the pro- portions of Polystira species with non-planktonic vs planktonic larval develop- ment will be essential for disentangling the relative importance of intrinsic and extrinsic factors in the generation of species diversity over varying spatial and temporal scales. Many studies have indicated that life history strategies of a wide variety of marine invertebrates have diverged across the Isthmus of Panama, with non-planktotrophic larvae with poorer dispersal capabilities (probably correlat- ing with short range distributions and increased speciation rates; Gaston 1994) today occurring more commonly in the Caribbean relative to the East Pacific (e.g., Jackson et al. 1996, reviewed in Lessios 2008). Within clades, these patterns like- ly evolved in response to the changed oceanographic conditions associated with isthmian closure. Studies of prey specificity at a range of hierarchical levels within the Polystira radiation also would be invaluable in understanding the role of feed- ing-related intrinsic factors in its distribution and diversification dynamics. Similarly, additional combined paleontological and neontological studies of species-level diversity patterns in other tropical American conoideans and other specialized carnivorous gastropods, might reveal how far we can go beyond clear changes in availability of preferred habitats and substrata (Vermeij and Petuch 1986) in explaining their widely differing post-isthmian fates. In this respect Conus offers great promise as a comparative system: Recent species are well sam- pled and the fossil TWA species, including those occurring in the same samples as Polystira, are beginning to be systematically revised (Hendricks 2008).

Conclusions

Our examination of evolution and extinction in Polystira has important impli- cations both for studies related to taxonomic diversity of conoideans—living and fossil—and the sorts of paleobiological questions we can ask of species-rich and rare taxa in the fossil record. The Conoidea are perhaps the most species-rich and among the most taxo- nomically under-described clades of marine gastropods (Bouchet et al. 2009). Our analyses have revealed that Polystira is speciating perhaps faster than any other species-rich marine gastropod clade so far analysed, including the Conidae. This suggests that for research into fine-scale evolution of conotoxins it would be ad- visable to conduct a detailed integrative study of living and fossil representatives of the focal taxon, whether in the selection of a target clade or as an integral part of the research. The very short species durations recorded in this study sug- gest that detailed paleontological research of other conoidean clades should be todd and johnson: caribbean gastropod species radiation dynamics 899 undertaken to help determine the generality of these patterns and inferred evolu- tionary dynamics in the superfamily. Compared to other studied benthos in the TWA, Polystira shows a lack of strong pulses of origination and extinction over the past 12 My—perhaps excluding a pulse in origination in the past 1.6 My. This suggests that intrinsic factors, such as feeding specialization and associated conotoxin evolution, may be relatively more important in establishing (and maintaining) high species diversity over time than extrinsic factors such as paleoenvironmental perturbation. Further support for this would be fruitfully sought in toxinological and feeding studies in Polystira. Combined neontological and paleontological analysis of selected conoidean clades over a range of biogeographic realms (e.g., tropical western Atlantic, Indo-West Pacific) would enable us to determine to what extent there might be geographical differences in the relative importance of regional environmental change (extrinsic drivers) and intrinsic drivers in the generation of hyperdiversity. This study emphasizes the importance of large-sized and replicated specimen samples with precise stratigraphic dating for outlining paleodiversity and evolu- tionary dynamics of hyperdiverse clades. Nevertheless, for many species compris- ing the long tail of rarity, limited numbers of recovered fossil specimens is likely due to original rarity and its macroecological correlates of short geographic and geologic range distributions (Gaston 1994). This expected ecological patchiness will be further exacerbated by collection bias, taphonomic (fossil preservational) factors, and the inevitable patchiness of the preserved and exposed rock record. Due to the many, poorly sampled, “rare” species expected within hyperdiverse mollusc clades, accurately estimating species durations or speciation rates across the full breadth of such a radiation appears impractical, as too is determining ab- solute species diversity within those clades across geologic time. Incorporating the fossil record into phylogenetic studies of species-rich radia- tions will lead us to examine how patterns of abundance and rarity are distributed across a phylogenetic tree, and to ask to what extent they may be phylogenetically conserved? If, as we expect, rarity in taxa like Polystira can be predicted from its correlation with phenotypic traits, then it should be possible to ensure that we fo- cus our detailed evolutionary questions on the more completely sampled (extinct and extant) and, we would infer, most robust subclades within molecular trees. Finally, within the TWA, detailed patterns of biotic turnover through the Neogene are still restricted to a few regions. Over recent years, geochronologi- cal control has in places become much more refined, to the point that we can begin to determine the extent of local variability of biotic response in timing and geographic expression, questions that were previously unanswerable (Jackson and Budd 1996). Throughout its range,Polystira is generally both abundant and diverse, notably in the Neogene formations of the Cibao Valley, Dominican Republic. This provides the prospect of inter-regional comparisons that may reveal more about both the factors controlling Polystira species diversity patterns in space and time, as well as contributing to our wider understanding of the geographic expression of biotic response to environmental change within tropical America. 900 BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013

Acknowledgments

We thank the numerous Panama Paleontology Project scientists and the staff of STRI, Panama, that have assisted in collecting, sorting, and curating masses of new fossil and recent material from Panama and Costa Rica. Above all we thank A Coates, J Jackson, and H Fortunato (STRI), and A Heitz, P Jung, and R Panchaud (NMB, Basel). R Collin and F Rodriguez (STRI) kindly made collections of Recent shell and alcohol-preserved speci- mens of Polystira from Panama for JAT. T Rawlings (Cape Breton University, Nova Scotia) worked closely with JAT acquiring much of the Recent data and imaged many of the Recent specimens. The following curators and collection managers kindly gave ATJ access to their collections and offered repeatedly extended loans: M Coppolino (ex-AMNH), N Voss (RSMAS), A Heitz, R Panchaud, W Etter, and O Schmidt (NMB), A MacLellan and K Way (NHMUK), P Greenhall, J Harasewych and the late W Blow (USNM). F Rodriguez loaned JAT material from STRI’s collections. A O’Dea (STRI) kindly invited us to the colloquium “Ecological and Evolutionary Change in Tropical American Seas over Broad Time-Scales” in Bocas del Toro, October 2011, from which this paper emerged. Research was supported by NERC Standard Research Grant GR3/13110 (Co-PIs: J Todd and R Thomas) and the Natural History Museum, London. J Hendricks (San José State University, CA, USA), A O’Dea, and two anonymous reviewers provided many helpful comments.

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Date Submitted: 6 November, 2012. Date Accepted: 27 May, 2013. Available Online: 20 August, 2013.

Addresses: (JAT) Department of Earth Sciences, Natural History Museum, London SW7 5BD, United Kingdom. Email: . (KGJ) Department of Earth Sciences, Natural History Museum, London SW7 5BD, United Kingdom. Email: .