Systematics, phylogeny and biogeography of the ...

JOl.JRNAL OF NATURAL HISTORY, 1990,24, 987-1026

Systematics, phylogeny and biogeography of the genus Mel/ita (Echinoidea: Clypeasteroida) ANTONY S. HAROLDt AND MALCOLM TELFORDt Department o/Zoology. University o/Toronto, Toronto, Ontario, Canada M5S1Al (Accepted27 November 1989)

The genus Mellita is an assemblage of New World tropical to temperate lunulate sand dollars (MeUitidae). Multivariate analysis of morphometric data, rep­ resenting specimens from Nantucket to Brazil, indicates the presence of three allopatric Atlantic species. The taxonomic history of Atlantic species has been traced from 1734 to the present. The following revisions of the Atlantic taxa are necessary: (I) Mellita isometra sp. nov., restricted to the east coast of North America, from Nantucket to Florida; (2) M. teflUis Clark, 1940 (west Florida to Louisiana) raises a previously described variety to species level. The type species, M. quinquiesper/orata (Leske, 1778) occurs from Louisiana to Brazil, including the Greater Antilles. Within the Pacific there are distinct species with extensively overlapping distributional ranges: M. longifissa Michelin, 1858; M. grantii Mortensen, 1948; M. notabilis Clark, 1947 and M. kanakofJi Durham, 1961. The Atlantic species do not form a monophyletic group. Phylogenetic analysis shows that the southerly form, M. quinquiesper/orata, is the sister group to a monophyletic group containing all of the Pacific species. The species of Mellita have probably originated through vicariance of a wide-spread ancestral biota in the late Neogene. KEYWORDS:

Mellitidae;

phylogeny;

historical

biogeography;

multivariate

analysis.

Introduction . The family Mellitidae is composed of three genera of New World, shallow water, lunulate sand dollars or keyhole urchins, Encope (including Mellitella), Leodia and Mellita, Species of Mellita occur in the Atlantic and Gulf of Mexico, from Nantucket to Brazil, and in the Pacific from the Gulf of California to Ecuador (Mortensen, 1948). The taxonomy of this very familiar genus has been in a state of remarkable confusion for some 250 years. For example, Ghiold and Hoffman (1984) assl,lmed that there was a single species- of Mellita in the Atlantic and invoked the idea of long-range dispersal to explain distribution. Ebert and Dexter (1976) separated two Pacific species (M. qrantii and M. longifissa) using morphometric analyses, but two other species (M. notabilis and M. kanakoffi), frequently misidentified as M.longifissa, were not included in their study. The genus was originally established by Klein (1734) to include two species, M, laevis and M. testudinata. Leske (1778) renamed these Echinodiscus bisper/oratus and

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A. S. Harold and M. Telford

E. quinquiesperforatus, respectively. The latter species has, at one time or another, been placed in five genera with any of nine different trivial names. The genus was resurrected by L. Agassiz (1841) and in 1956 the International Commission on Zoo­ logical Nomenclature, by designation under its plenary powers, placed Mellita Agassiz (J.L.R.), 1841 on the official list of generic names with Echinodiscus quinquiesperJoratus Leske, 1778 as the type species. During its taxonomic history the genus has contained five- as well as six-Iunuled sand doUars. In 1851 Gray (cited by Mortensen, 1948) erected the genus Leodia for the six-Iunuled forms, L. sexiesperJorata (Leske, 1778) as the type species. This new genus was not recognized by Agassiz (1874) and remained a junior synonym of Mellita until it was revived by Lambert and Thiery (192\). It has subsequently been widely accepted (Clark, 1940; Cooke, 1942; Serafy, 1979) although Mortensen (1948) regarded Leodia as a subgenus of Mellila. In the present study we point out the principal differences between Mellita and Leodia. Recent five-Iunuled species are all referrable to the genus Mellita, whilst Leodia contains a single good species, L. sexiesperJorata (Leske). In addition, there are three problematical six-lunuled extant forms which have variously been assigned to one or the other of these two genera. These are not considered Mellita species here and will be discussed separately following the phylogeny section. Considerable diversity of form exists among Atlantic Mellita but A. Agassiz (1872~74) regarded all of them as a single species (Klein's M. testudinata). Clark (1940) disagreed: he thought that there were three species, one of which was represented by two varieties. Unfortunately, he failed to recognize that one of his new species was Klein's original species, as we shall show. Taxonomic opinion has not supported Clark and, following Mortensen's lead (1948), his species have been regarded merely as varieties (for example, see Serafy, 1979). In our opinion there are three Atlantic species, recognizable both by eye and by multivariate analysis, and each with its own distinct geographical range. We have traced the nomenclatural history from the original species description of 1734 (Klein) to the present. Although Clark (1940) was therefore mostly correct in his perception of forms, he was wrong in his designations of species. Amongst the Pacific members of the genus there is much less systematic confusion. There are four species (M. grantii, M. longifissa, M. notabilis, and M. kanakoffi), with extensively overlapping ranges. However, there has been some confusion in identification and two of the species (M. notabilis Clark, 1947 and M. kanakoffi Durham, 1961) have been almost totally overlooked by subsequent investigators. Following revision of the seven extant species, we provide a key for their identification. Through cladistic analysis we develop a phylogenetic hypothesis which shows that on their own the Atlantic species do not constitute a monophyletic group, but the Pacific species do. The biogeographical implications of the phylogeny are then discussed. Materials and Methods Material Examined Sand dollars were examined from sites spanning the entire geographical range of extant Mellita species, listed by species in the systematic section (institutional abbreviations for loaned material are given in Leviton et al., 1985, with the exception of the University of California Museum of Paleontology, UCMP). This paper is

Mellita: Systematics, Phylogeny, Biogeography

989

concerned solely with Recent species and we shall make only passing reference to fossil taxa. Morphometry The statistical analysis investigates variation and the problem of discrimination of the Atlantic representatives of Mellita. We use multivariate methods to test our classification of Atlantic forms. In doing so we assume that species can be recognized phenetically, even if highly variable. Many studies have indicated that some echinoderms exhibit developmental plasticity (Marcus, 1983). Stanton et al.(1979) show that populations of the west coast sand dollar, Dendraster excentricus, display particular morphologies that are apparently correlated with environmental parameters. The problems inherent in delimiting variable species are not unique to multivariate treatments but, rather, pose a difficulty in systematics. When the full range of habitats is sampled the morphological range of ecophenotypes ought to be continuous. Therefore it should be possible to delimit species in multivariate space provided that the geographic and ecological ranges are well-sampled. A series of morphometric measurements was chosen in order to assess variation in test shape, positions and dimensions of the lunules and width of the pressure drainage channels (terminology of Telford, 1983). The variables and their abbreviations (see Figs I and 2) are listed below. Numbering follows Loven's system (1892), in which ambulacra bear Roman and interambulacra Arabic numerals.

ABORAL St:RFACE

ORAL SURFACE

Fig. 1. Main features of Mel/ita, aboral surface. Alpha-numeric codes refer to rays of Loven (1892). Areas enclosed by solid lines are lunules; elongate stippled areas, petaloids; central pentagon, madreporite; solid triangles, locations of test thickness measurements. FIG. 2. Main features of Mellita, oral surface. Radiating bifurcate lines are food grooves; stippled areas, pressure drainage channels; mouth, central, and encircled by basicoronal plates; periproct immediately posterior of mouth.

1. L. Test length: from ambitus at ambulacrum III (anterior) to ambitus at inter­

ambulacrum 5. 2. W. Test width: perpendicular to anterior-posterior axis at midpoint. 3. A-I, A-II, A-III. Ambulacrallengths: along perradii from margin of peristome to ambitus.

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A. S. Harold and M. Telford

4. 1-3,1-4,1-5. lnterambulacrallengths: along interradii from margin ofperistome to ambitus. 5. ALL-IV, ALL-V. Ambulacrallunule lengths: measured on aboral surface. 6. ALW-IV, ALW-V. Ambulacrallunule widths: measured at midpoint oflunules. 7. ALP-IV, ALP-V. Ambulacrallunule positions: distance from adapical margin of lunule to centre of madreporite. 8. PO-Ill, PO-IV, PO-V. Pressure drainage channel spans: maximum distance between primary food grooves. 9. LPl, LP2, LP3, LP4, LP5, LP6, LP7. Longitudinal profile: lest thickness at seven equidistant points along longitudinal axis, starting at ambitus. 10. TPI, TP2, TP3. Transverse profile: test thickness along left half of transverse axis, midway along longitudinal axis. II. MAXT. Maximum thickness: maximum vertical test thickness in an­ terior-posterior axis. 12. POSMAXT. Position of maximum thickness: distance of MAXT from anterior ambitus. 13. ANLUNL. Anal lunule length: measured on aboral surface. 14. ANLUNW. Anal lunule width: measured at midpoint oflunule. IS. ANLUNP. Anal lunule position: distance from adapical margin of lunule to centre of madreporite. 16. POSAP. Position of apical system: distance from centre of madreporite to ambitus in ambulacrum III. The above measurements were subjected to a base 10 logarithmic transformation before statistical treatment. Untransformed measurements, converted to proportions of test length (L), are summarized for each species in the systematics section. Specimen size given in figures and text is test length throughout. Statistical Procedures SAS (Statistical Analytical Systems, Inc.) multivariate ordinating procedures were applied to a correlation matrix derived from the log-transformed test measure­ ments. The reader is directed to Thorpe (1976) and Albrecht (1980) for discussion of assumptions and applicability of the methods that we have used. To minimize the effect of size-related variation, a subset of specimens (length 40 to 85 mm) formed the basis of the data set. Principal components analysis (PROC FACTOR was used to examine the possibility of intergradation between the Atlantic taxa as well as patterns of geographical variation within them. Between taxon variation can be ordinated by canonical discriminant analysis (Albrecht, 1980) through PROC CANDISC and the likelihood of group membership can then be tested by discriminant analysis (PROC OISCRIM). This is a valuable test of results from the principal components analysis and the classification that we are proposing. For this analysis specimens were assigned a priori to classes (taxa) using some of Clark's criteria (1940). We were unable to distinguish between his M. lata and Jl. latiambulacra. Specimens wcre therefore assigned to three groups on the basis of geographic occurrence (for discussion of the results these groups will be referred to by letter): A: East coast of North America (Clark's 'typical' M. quinquiesperforata). B: Eastern Gulf of Mexico (Clark's M. q. vaL tenuis). C: Western Atlantic shelf from Mississippi Oelta through Central and South American coasts to Brazil (Clark's M. lata plus M. latiambulacra).

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Mellita: Systematics, Phylogeny, Biogeography

A priori classification of the specimens according to their geographical distribution avoids potential circularity of argument when the classification is subsequently tested by morphometric analysis. Statistical Results Within Group Variation The bulk of the variation within group C is summarized by ordinating the first two factors of the PCA (Fig. 3). They account for 41 % and 32% of the variance, respectively, and have eigenvalues of 12.82 and 9.99. These two factors account for nearly three-quarters of the variance, and were the only ones for which loadings were interpreted. The third and fourth factors were examined, but they account for a relatively small part of the variance and provided no useful addition to the analysis. The loadings (squared correlations) of the original variables on the first two factors are listed in Table L In Fig. 3, factor 1 (horizontal axis) is correlated with a com­ bination of ambulacral and lunule position measurements, whereas factor 2 (vertical Table I. Variable loadings on the first two factors of PCA of group C sand dollars (Clark's M. lata and M. latiambulacra, western Gulf of Mexico, Central and South America, Greater Antilles). '" Tndicates variables with highest loadings. Variable

Factor I

Factor 2

L W A-III A-IV A-V 1-3

0.7260 0.6860 0.7322 0.6982 0.7032 0.7375 0.6854 0.7127 0.4526 0.5137 0.4743 0.3904 0.7775* 0.7532* 0.7207 0.7516* 0.7587* 0.4122 0.5811 0.6049 0.6167 0.5617 0.4216 0.2542 0.4162 0.5438 0.5608 0.6132 0.6409 0.2333 0.7749* 0.7348 0.7323

0.5146 0.5038 0.5502 0.5038 0.4876 0.5196 0.5229 0.5049 0.4238 0.3855 0.4034 0.3433 0.5243 0.5098 0.3785 0.1976 0.2870 0.7521 '" 0.6106 0.6127 0.6302 0.6785 0.7708* 0.8647* 0.8061* 0.7204* 0.6609 0.6085 0.4564 0.2632 0.4998 0.5117 0.4546

1-4

1-5 LL-IV LL-V LW-IV LW-V ALP-IV ALP-V P~-III

PO-IV PO-V LPI LP2 LP3 LP4 LP5 LP6 LP7 TPI TP2 TP3 MAXT ANLUNL ANLUNW ANLUNP POSAP POSMAXT

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A. S. Harold and M. Telford 4.0

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