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Adaptive Zones and the Pinniped Ankle: a 3D Quantitative Analysis of Carnivoran Tarsal Evolution

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Adaptive Zones and the Pinniped Ankle: a 3D Quantitative Analysis of Carnivoran Tarsal Evolution Polly, P. D. 2008. Adaptive Zones and the Pinniped Ankle: A 3D Quantitative Analysis of Carnivoran Tarsal Evolution. Pp.167-196 in (E. Sargis and M. Dagosto, Eds.) Mammalian Evolutionary Morphology: A Tribute to Frederick S. Szalay. Springer: Dordrecht, The Netherlands. ADAPTIVE ZONES AND THE PINNIPED ANKLE A three-dimensional Quantitative Analysis of Carnivoran Tarsal Evolution P. DAVID POLLY Department of Geological Sciences Indiana University 1001 East 10th Street Bloomington, Indiana USA [email protected] Abstract The form-function complex comprised of calcaneum and astragalus was studied in twelve extant carnivorans using a new morphometric technique for analysis of three-dimensional surfaces. The study sample included eleven fissipeds representing the phylogenetic and functional diversity of terrestrial Carnivora plus one pinniped, Phoca. A redefined adaptive zone concept was used to explain the relative effects of ecological adaptation and common ancestry in phylogeny reconstruction from quantitative morphological data. As used here, an adaptive zone is a bounded range of phenotypes linked to specific functional roles, a definition that emphasizes morphology rather than environment or fitness. The following criteria were proposed for testing for the existence of an adaptive zone: (1) the zone must be occupied by real taxa; (2) their phenotypes must lie within a limited morphospace whose major axes are associated with functional factors; (3) the zone’s occupants must have diversified throughout the zone without crossing its boundaries except through a major change in lifestyle, and (4) phenotypes that lie outside the zone must be functionally incompatible with the functions associated with the zone axes. Criterion 3 requires that the phylogeny of the group be independently known, at least in part. The shape of the calcaneum and astragalus were analyzed using a new technique for 3D surfaces. Bone surfaces were represented as a quadrilateral grids of points applied to the surface of the scanned object. The technique for placing the grid was modified from Eigenshape outline analysis. The point grids were superimposed using Procrustes ordination and analyzed using the standard statistical procedures used in analysis of Cartesian landmarks. The new method allows results to be illustrated as shaded three-dimensional bones rather than constellations of landmarks or numeric data tables. Variation in tarsal morphology was found to be associated with stance, number of digits, and locomotor type. The long held opinion that intertarsal mobility is enhanced by disparity in size and curvature of occluding facets was not supported. Ancestral morphotypes of the calcaneum and astragalus were reconstructed using GLM algorithms. The reconstruction at the base of the carnivoran tree had a morphology compatible with five digit, digitigrade or semidigitigrade terrestrial locomotion, a hypothesis consistent with the earliest carnivoran fossil taxa. Fissiped tarsals fell within an adaptive zone whose major phenotypic axes were associated with intertarsal mobility, stance, and locomotor type. During their phylogenetic history, fissiped clades crossed the adaptive zone space many times as different clades convergently evolved locomotor specializations. The only lineage to pass through the boundaries of the adaptive zone morphospace was that leading to the pinniped Phoca. Pinnipeds acquired their derived morphology by colonizing new regions of shape space, but not by evolving more quickly than fissiped clades. Evolution within the adaptive zone is an example of an Ornstein- Uhlenbeck process, which erases deep phylogenetic history. Consequently, phylogenetic patterns are unlikely to be accurately reconstructed from quantitative representations of tarsal shape for species whose last common ancestor is older than 5 to 15 million years. Keywords: adaptive zones, ancestral node reconstruction, Carnivora, phylogeny reconstruction, tarsals, 3D morphometrics ADAPTIVE ZONES AND THE EVOLUTION OF PINNIPEDS 2 Introduction History repeats the old conceits, the glib replies, the same defeats Elvis Costello (1982), Beyond Belief Bones are functional. Stated so abruptly, this skeletal characters are functional – they are – observation is a truism, but its significance but to what extent adaptation masks depends on the context in which it is made. In phylogenetic history, how the convergences can an individual animal, bones support loads, resist be recognized, whether adaptation impedes muscular contractions, and facilitate bodily phylogeny reconstruction, and how the movements. Bone form both constrains, and is interplay between form, function, and shaped by, force and motion. In an phylogeny can be better understood. These environmental context, a bone’s form is questions are the main subject of this paper. compatible with its owner’s size and habits and In this paper, function and phylogeny were is, thus, related indirectly to habitat and analyzed using a new geometric morphometric environment, although any particular bone (or, technique that quantitatively represents the more properly, musculoskeletal configuration) entire three-dimensional surface of the bones. can cope in diverse environments, and any This method was used to associate variation in substrate can be traversed by animals with the two bones, including the size and curvature different skeletal forms. Form and function are of occluding joint facets, with locomotor type, inseparable at the level of joint movements stance, number of digits, and body mass. (Bock and von Wahlert, 1965), but they are Principal components analysis was used to only loosely correlated at the level of ecology, describe the major axes of variation in the two specifically locomotor types and habitats. The bones, and multivariate analysis of variance was coarseness of the correlation between form and used to test functional categories for ecology come from the temporal lag of significance. Correlated transformations in the phylogenetic adaptation and the many-to-many interlocking surfaces of the two bones were also relationship between form and habitat. Even explored using two-block partial least squares. though ecophenotypic plasticity allows bones to Phylogenetic components of variation were be modified during an individual’s lifetime, assessed by mapping the three-dimensional bone form is largely heritable and evolutionary shape of the bones onto a cladogram and change requires generations of selective genetic projecting the results back into the principal and epigenetic reorganization (Cock, 1966; component morphospace to visualize the Grüneberg, 1967; Thorpe, 1981). patterns of homoplasy. Rates of morphological Some have argued that functional evolution in the several clades were calculated adaptation is incompatible with phylogenetic from the mapped shapes. Homoplasy was also reconstruction. Assertions as to whether quantitatively assessed by measuring the skeletal variation is primarily phylogenetic scaling coefficient between evolutionary (Acero et al., 2005) or functional (Nadal- divergence and time since common ancestry. Roberts and Collard, 2005) color the entire The final aim of this paper was to develop canon of systematic literature, but the nature of criteria for assessing the whether functional the conflict is murky – functional adaptation is adaptation is likely to confound phylogenetic a phylogenetic process and the phylogenetic signal in a dataset for the taxa being considered. transformation of bone form does not occur A quantitative redefinition of Simpson’s outside a functional context. On one hand, all adaptive zones was employed to assess the adaptive specializations, even those shared by effect of adaptive convergence on phylogenetic different clades, arise phylogenetically, but on divergence, and determine the circumstances in the other, no bone character is functionally which associated homoplasy is likely to neutral. The question, then, is not whether confound phylogeny reconstruction. 3 P. DAVID POLLY ADAPTIVE ZONES, FUNCTION, AND another will do so by evolving a new phenotype PHYLOGENY compatible with its new environment; those that do not escape will remain constrained within Adaptive zones are arguably the key to the zone’s range of phenotypes. The adaptive interpreting the relationship of form, function, zone underpinned Simpson’s (1945) taxonomic and phylogeny. Simpson (1944, 1953) concept of a phenotypically coherent, introduced the concept of adaptive zones for paraphyletic group, and rejection of that environmental spaces that accommodate several concept by cladists in the 1970s conflated evolving lineages. Species inside a zone have adaptive zones and plesiomorphic characters latitude for phenotypic evolution and (Rosen, 1974). During the same period, speciation, but those that evolve too near the quantitative geneticists developed sophisticated zone’s margins are normally weeded out by mathematical models of adaptive peaks, selection. Simpson hypothesized that new adaptive landscapes, and trait covariances that zones are colonized when rapid bursts of are conceptually related to adaptive zones, but ‘quantum’ evolution propel a species across the whose focus was not taxonomic (Lande, 1976, selectively disadvantageous space between 1986; Kirkpatrick, 1982; Wake et al., 1983; zones. Any lineage that escapes one zone for Wright, 1988; Cheverud, 1996; Schluter, 1996; Figure 1. Skeleton of Canis familiaris, the Domestic dog (A) and Phoca vitulina, the Harbour seal (B). (After Gregory,
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