Sandra J. Carlson

The muricid gastropod subfamily Rapaninae: phylogeny and ecological history

Abstract Members of the neogastropod muricid subfamily Rapaninae are abundant, shallow-water predators whose phylogeny was previously investigated by Kool (1993b), who used mainly anatomical characters. In order to deepen understanding of the evolution of this important clade and to incorporate functional, ecological, and fossil evidence, we performed a phylogenetic analysis based on 34 shell characters in 45 genus-level taxa, including five muricid outgroups. Cladograms based on shell characters alone differed from those founded on anatomical features, and these analyses differed from the phylogenetic reconstruction combining all available morphological evidence. The preferred cladogram incorporates all evidence and reveals a “Thais group” and an “Ergalatax clade” that both emerge from the derived portion of a more primitive, paraphyletic group of other rapanines. The Ocenebrinae, the other four outgroup taxa, and three ergalataxine taxa all lie outside the rapanine clade that includes the remaining ergalataxines as a derived subclade. We used the phylogenetic results to probe aspects of the ecological history of the Rapaninae. Our data imply that antipredatory shell defenses (elongated aperture, denticles on the inner side of the outer lip, and robust external spines and tubercles) evolved multiple times, mainly in post–early Miocene clades in the Indo–West Pacific region. These results support earlier nonphylogenetic inferences. We compared known prey types and methods of predation of living rapanines with their distribution on our phylogenetic tree. The plesiomorphic mode of feeding in the Rapaninae is drilling of hard-shelled prey. Feeding by other means and on such soft-bodied prey as sipunculan and polychaete worms evolved several times independently among post–early Miocene rapanines in the Indo–West Pacific. Methods of predation on hard-shelled prey that involve edge-drilling or attack by way of the aperture also evolved independently several times, but did so throughout the geographical range of the subfamily. Specialization for life on the upper shore occurred in at least eight lineages, all but two of which are confined to the Indo–West Pacific. Ecological diversification of the Rapaninae was therefore most common in the tropical Indo–West Pacific during and after early Miocene time. This diversification occurred in a setting of already high biological diversity and intense competition and predation.

Phylogenetic relationships among extant brachiopods

Abstract— The monophyletic status of the Brachiopoda and phylogenetic relationships within the phylum have long been contentious issues for brachiopod systematists. The relationship of brachiopods to other lophophore‐bearing taxa is also uncertain; results from recent morphological and molecular studies are in conflict. To test current hypotheses of relationship, a phylogenetic analysis was completed (using PAUP 3.1.1) with 112 morphological and embryological characters that vary among extant representatives of seven brachiopod superfamilies, using bryozoans, phoronids, pterobranchs and sipunculids as outgroups. In the range of analyses performed, brachiopod monophyly is well supported, particularly by characters of soft anatomy. Arguments concerning single or multiple origins of a bivalved shell are not relevant to recognizing brachiopods as a clade. Articulate monophyly is very strongly supported, but inarticulate monophyly receives relatively weak support. Unlike previous studies, the nature of uncertainties about the clade status of Inarticulata are detailed explicitly here, making them easier to test in the future. Calcareous inarticulates appear to share derived characters with the other inarticulates, while sharing many primitive characters with other calcareous brachiopods (the articulates). Experimental manipulation of the data matrix reveals potential sources of bias in previous hypotheses of brachiopod phylogeny. Although not tested explicitly, lophophorate monophyly is very tentatively supported. Molecular systematic studies of a diverse group of brachiopods and other lophophorates will be particularly welcome in providing a test of the conclusions presented here.

Examining the latitudinal diversity gradient in Paleozoic terebratulide brachiopods: should singleton data be removed?

Abstract Studies of taxonomic diversity over time commonly count and compare first- and last-appearance data (FADs and LADs) over a succession of temporal intervals, and interpret them with respect to taxon origination and extinction. Singleton taxa, which first appear and last appear in the same temporal interval, are often removed from analyses because they might result from preservational biases rather than evolutionary processes, or they might represent non-independent FADs and LADs. Should singleton taxa always be excluded? We argue that in the case of Paleozoic terebratulide brachiopods, although they may be sensitive to biases in sampling intensity, singleton genera should be included in diversity studies because they do not appear to result from more typical biases, such as Lagerstätten and temporal interval length, that arguably can result in artificially high numbers of singleton genera. Singleton genera can be critical and effective when used to test hypotheses regarding the existence and generation of latitudinal diversity gradients. Contrary to the anti-tropical diversity pattern of modern articulated brachiopods, Paleozoic terebratulides show a latitudinal diversity gradient that peaks in the Tropics. The hypothesis that the Tropics are either a diversity source or sink can be tested by comparing FAD and LAD latitudes. For singleton genera, FAD and LAD latitudes are taken from the same data points and must be removed for statistical comparisons to be valid. We suggest that taxon age distributions can accommodate singleton data, as the taxon age metric considers origination and extinction simultaneously. We generated taxon age distributions to test the hypothesis that the observed Paleozoic diversity gradient results from a latitudinal bias in generic turnover rate. We discovered that singletons are not randomly distributed over latitude, with proportionally more singleton genera occurring in the Tropics. In this case, singleton genera may reflect rapid evolutionary turnover of taxa, rather than simply preservational bias. Methods that can accommodate singleton taxa should be used to study the diversity of Paleozoic terebratulides and possibly other well-skeletonized marine metazoans.

How phylogenetic inference can shape our view of heterochrony: examples from thecideide brachiopods

Abstract Heterochrony is considered to be an important and ubiquitous mechanism of evolutionary change. Three components are necessary to describe heterochrony: phylogenetic relationships, size and shape change, and timing of developmental events. Patterns and processes of heterochrony are all too often invoked before all three components have been investigated. Phylogenetic hypotheses affect the interpretation of heterochrony in three ways: rooting of a clade, topology of a clade, and character polarity. To study these effects we examined the distribution of shell microstructure, lophophore support structures, and body size in four different phylogenetic hypotheses of thecideide brachiopods (Triassic to Recent), a group of minute, cryptic, benthic marine invertebrates. Thecideides are consistently monophyletic in experiments using terebratulide, strophomenate, and spire-bearing outgroups together and separately, varying ingroup membership, and experimentally withholding certain character complexes. Thecideide monophyly is also supported by bootstrap analysis. Hypotheses of heterochrony in thecideide origins and evolution are therefore not merely artifacts of classification and can be pursued further. Using either strophomenate or spire-bearing outgroups, Triassic Thecospira is the most primitive thecideide. Trees constructed using terebratulide outgroups are rooted instead at Eudesella, a taxon derived in every other phylogenetic reconstruction, and the Triassic thecideides occupy derived rather than primitive positions. Our phylogenetic results support the traditional interpretation of the reduction or loss of the secondary fibrous shell layer as a paedomorphic pattern, whereas the evolution of lophophore support structures suggests a peramorphic pattern. Reduction in thecideide adult body size is gradual, phylogenetically, and results in an overall paedomorphic pattern. Heterochrony in these three character suites may play a role in the subsequent evolution of the clade, but apparently not in the origin of the clade, as is commonly thought. Heterotopy, rather than—or in addition to—heterochrony, may account for both the origin and evolution of the lophophore support structures and in the reduction and loss of the secondary shell layer. These phylogenetic hypotheses suggest that heterochrony can result from a complex mosaic of processes and provide specific, testable predictions about the processes responsible for producing the patterns, whether heterochronic or not. Categorizing an entire clade (such as thecideides), rather than individual characters, as globally paedomorphic may allow interesting peramorphic patterns in individual characters to be overlooked.

Evidence for the Early Oligocene formation of a proto-Subtropical Convergence from oxygen isotope records of New Zealand Paleogene brachiopods

Abstract Using the oxygen isotope record in fossil brachiopods, we reconstruct Late Eocene through Early Miocene paleotemperatures of an eastern New Zealand shelf environment. Our results show a decline in temperature to a low of ∼6°C in the Early Oligocene, of a magnitude similar to that of open-ocean isotopic studies from similar latitudes. However, the brachiopod-derived paleotemperatures are ∼ 10°C lower than those inferred from occurrences of warm-water fauna and flora (e.g., large foraminifera, mangrove and coconut palms), which suggest a subtropical (20–23°C) climate throughout most of the New Zealand Oligocene. We propose that a proto-Subtropical Convergence (pSTC), with cool subantarctic water flowing along the eastern coast of the South Island, first developed in the Early Oligocene. The subtropical fauna and flora distribution patterns are consistent with this hypothesis. Warm-water biota (e.g., larger foraminifera, and mangrove trees) occur primarily on the west and north coasts of New Zealand in warm subtropical water characteristic of water north of the pSTC, similar to the modern Subtopical Convergence. We explain the occurrence of occasional subtropical taxa in Early Oligocene strata of the east coast of the South Island as a result of the north-south migration of the pSTC or the colonization of relict Surtseyan-type seamounts in local waters warmed by volcanic eruptions.

Phylogenetic signal in extinction selectivity in Devonian terebratulide brachiopods

Abstract Determining which biological traits affect taxonomic durations is critical for explaining macroevolutionary patterns. Two approaches are commonly used to investigate the associations between traits and durations and/or extinction and origination rates: analyses of taxonomic occurrence patterns in the fossil record and comparative phylogenetic analyses, predominantly of extant taxa. By capitalizing upon the empirical record of past extinctions, paleontological data avoid some of the limitations of existing methods for inferring extinction and origination rates from molecular phylogenies. However, most paleontological studies of extinction selectivity have ignored phylogenetic relationships because there is a dearth of phylogenetic hypotheses for diverse non-vertebrate higher taxa in the fossil record. This omission inflates the degrees of freedom in statistical analyses and leaves open the possibility that observed associations are indirect, reflecting shared evolutionary history rather than the direct influence of particular traits on durations. Here we investigate global patterns of extinction selectivity in Devonian terebratulide brachiopods and compare the results of taxonomic vs. phylogenetic approaches. Regression models that assume independence among taxa provide support for a positive association between geographic range size and genus duration but do not indicate an association between body size and genus duration. Brownian motion models of trait evolution identify significant similarities in body size, range size, and duration among closely related terebratulide genera. We use phylogenetic regression to account for shared evolutionary history and find support for a significant positive association between range size and duration among terebratulides that is also phylogenetically structured. The estimated range size–duration relationship is moderately weaker in the phylogenetic analysis due to the down-weighting of closely related genera that were both broadly distributed and long lived; however, this change in slope is not statistically significant. These results provide evidence for the phylogenetic conservatism of organismal and emergent traits, yet also the general phylogenetic independence of the relationship between range size and duration.

GHOSTS OF THE PAST, PRESENT, AND FUTURE IN BRACHIOPOD SYSTEMATICS

Abstract Three historical phases can be distinguished in the study of brachiopod systematics over the past 75 years. Prior to 1956, systematic neontologists and paleontologists struggled to reconcile differences in perceived evolutionary patterns (and thus classifications) based largely on static morphological differences observed separately among living brachiopods and among fossil brachiopods. Following 1956, patterns of morphological distribution began to be interpreted relative to the processes by which they were formed, and a more dynamic view of brachiopod phylogeny and classification resulted. Over the past decade, newer methodologies (phylogenetic systematics) have allowed older phylogenetic hypotheses to be tested and evaluated. The major challenges that brachiopod systematists now face are not unique to brachiopods; they concern improving the methods of phylogeny (and classification) reconstruction so that all the sources of data available to paleontologists can be utilized more effectively. In the future, I predict that more intensified, global fossil collecting, together with further investigation of the embryology and development of brachiopods, and molecular systematic research, will play an increasingly larger role in revising the classification currently in use.

Predation on Modern and Fossil Brachiopods: Assessing Chemical Defenses and Palatability

ABSTRACT The post-Paleozoic decline of the diversity and abundance of rhynchonelliform brachiopods has been attributed to a variety of factors. Of the possible mechanisms invoked to explain the evolutionary decline and cryptic or antitropical distribution of brachiopods, predation has frequently been dismissed due to the potentially low energetic value and suspected nonpalatability or toxicity of brachiopod tissues. Herein we demonstrate that multiple invertebrate marine predators (crustaceans, echinoderms, and gastropods) are willing and able to consume brachiopods in laboratory settings without observable negative effects after ingestion. In addition, field samples indicate predation pressure on the living brachiopod population may be substantial. Although feeding trials are consistent with previous reports that bivalves are preferred prey relative to brachiopods, predation should not be dismissed as a potentially important factor in brachiopod ecology and evolution. The results presented herein reveal that in some cases brachiopods may be the intended target of predatory attacks, especially in habitats where mollusks are rare or absent. Examination of the fossil record of predation on rhynchonelliform brachiopods is consistent with this interpretation: evidence for drilling and repair of brachiopod shells is found throughout the fossil record in multiple lineages. While it is likely that predation traces on post-Paleozoic brachiopods are generally rare, there are multiple reports of fossil localities with anomalously high drill-hole or repair-scar frequencies. This suggests that although brachiopods may be unwanted prey in the presence of energetically more desirable targets, they do appear to be edible and subject to intense predator-prey interactions under certain conditions.

Morphological analysis of phylogenetic relationships among extant rhynchonellide brachiopods

Abstract Rhynchonellida is the stratigraphically oldest and phylogenetically most basal of the extant rhynchonelliform brachiopod orders, yet phylogenetic relationships among rhynchonellides are poorly known. The fourteen named rhynchonellide superfamilies (four of which have extant representatives) were defined primarily on the basis of features of the dorsal cardinalia, particularly crural morphology, but their homology and polarity have not been investigated rigorously. Superfamily monophyly is unclear, as is the evolution of several distinctive rhynchonellide morphological features, such as crura. The purpose of this study is to investigate the phylogenetic relationships among extant rhynchonellide genera using skeletal characters, and to compare the results with the current classification, elucidating the evolution of morphological features in the process. We completed parsimony-based and Bayesian analyses using fifty-eight characters of the interior and exterior of the shell that vary among the nineteen extant genera. Our results are readily interpretable with respect to the classification, and indicate that Hemithiridoidea, Dimerelloidea, and (in some analyses) Pugnacoidea appear to be monophyletic. Species classified in Dimerelloidea and Pugnacoidea, and in certain cases Hemithiridoidea, each form derived subclades that evolve from within a paraphyletic Norelloidea at the base of each subclade. Raduliform crura appear to be the most basal, phylogenetically; five other crural morphologies evolve from the raduliform state. However, morphological characters currently uniting genera in rhynchonellide superfamilies are not clearly diagnostic and exhibit a relatively high degree of homoplasy overall, suggesting that consistency with the classification may be based on a false sense of confidence in rhynchonellide morphology to clearly elucidate evolutionary relationships. Published molecular phylogenetic hypotheses conflict with the morphological topologies, further supporting this possibility. The evolutionary trends among diagnostic characters of Recent rhynchonellides appear to reflect successive juvenilization in adult morphology in several subclades, suggesting that heterochrony may have played an important role in the evolution of the group.

Three-dimensional morphological variability of Recent rhynchonellide brachiopod crura

Abstract Crura, the calcareous support structures of the lophophore in rhynchonellide brachiopods, have historically been used to justify higher-level rhynchonellide classification and reveal major evolutionary lineages within rhynchonellides. Seventeen crural types have been described and categorized into four groups based on variation in overall structure and cross-sectional shape, but not evaluated in a quantitative or comprehensive manner. Heterochrony has been hypothesized to play a role in the evolutionary transitions among some types, but the structural, developmental, and phylogenetic context for testing these hypotheses has not yet been established. In this study, we use three-dimensional geometric morphometric techniques to quantify morphological disparity among all six crural morphs in Recent adult rhynchonellides, with the goal of delineating more objective criteria for identifying and comparing crural morphs, ultimately to test hypotheses explaining morphological transformations in ontogeny and phylogeny. We imaged the crura of seven Recent rhynchonellide species, using X-ray computed microtomography. We used landmarks and semi-landmarks to define the dimensions and curvature of the crura and the surrounding hinge area. Procrustes-standardized landmark coordinates were analyzed using a principal component analysis to test the discreteness of the individual crural morphs and named groups of morphs, and to identify features that vary most among the crural configurations. Our results demonstrate that microCT imaging techniques provide novel ways to investigate the morphology of small features that may be otherwise impossible to quantify using more conventional imaging techniques. Although we predicted overlap among crural morphs in the 3-D shape space, the principal component analyses suggest that five of the six crural morphs differ distinctly from one another. Some but not all previously designated crural groups appear to exhibit morphological cohesion. This study establishes a quantitative morphological foundation necessary to begin an investigation of the phylogenetic significance of ontogenetic changes in crura, which will allow hypotheses of heterochrony to be tested.