(Conoidea: Turridae: <I>Polystira</I>) Over 12 Million Years in the Sout

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(Conoidea: Turridae: <I>Polystira</I>) Over 12 Million Years in the Sout 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
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