Beckman Research Institute of the City of Hope, City of Hope Medical Center, Duarte, CA .... Progress in four areas of research will be summarised here: (1) DNA ...
Aust. J. Zool., 1990, 38, 535-54
Immunological Relationships and Generic Revision of the Australian Lizards Assigned to the Genus Leiolopisma (Scincidae :Lygosominae) Mark N. ~utchinson*,Stephen C. ~ o n n e l l a B,n Peter R. aver stock^', Malcolm ~ r i B, e Sally ~ simmsB and Shelly ~ u r g i n School of Biological Sciences, La Trobe University, Bundoora, Vic. 3083; present address: South Australian Museum, North Terrace, Adelaide, S.A. 5000, Australia. South Australian Museum, North Terrace, Adelaide, S.A. 5000, Australia. Present address: Centre for Coastal Management, University of New England, P.O. Box 157, Lismore, N.S.W. 2480, Australia. School of Biological Sciences, Macquarie University, N.S.W. 2109; present address: Department of Applied Sciences, University of Western Sydney, Hawkesbury, Richmond, N.S.W. 2753, Australia. A
Abstract The phylogenetic relationships of the Australian scincid lizards currently assigned to the genus Leiolopisma have been examined by quantitative micro-complement fixation (MC'F) comparisons of serum albumin. The results of these comparisons do not support the monophyly implicit in these species' current congeneric status, but suggest instead that the Australian species of Leiolopisma belong to several distinct phyletic lineages within the Eugongylus group. These findings are supported by several sets of non-biochemical characters, including features of scalation, osteology and karyotype. None of the Australian species shares a close relationship with the type-species of Leiolopisrna (L. telfairii), and so a new taxonomic arrangement is proposed which distributes them among the following genera: Bartleia, gen. nov. (jigurru); Bassiana, gen. nov. (duperreyi, platynotum and trilineata); Cautula, gen. nov. (zia);Niveoscincus, gen. nov. (coventryi, greeni, metallicus, microlepidotus, ocellatus, orocryptus, palfreymani and pretiosus); and Pseudemoia Fuhn, 1967 (baudini, entrecasteauxii Group 1 ; entrecasteauxii Group 2, rawlinsoni and spenceri). Preliminary comparisons suggest that other Leiolopisma species, from New Caledonia, Lord Howe I. and New Zealand, belong to phyletic lineages which are distinct from any of the Australian 'Leiolopisrna' and from the type-species.
Introduction The genus Leiolopisma has long been a major taxonomic unit in scincid systematics. First proposed as a subgenus of Gongylus by Dumeril and Bibron (1839), it originally included only L. telfairii, an endangered species restricted in modern times to Round I. off the coast of Mauritius (Arnold 1980). Leiolopisma was distinguished from the other smooth-scaled, normally proportioned skinks lacking supranasals (Dumeril and Bibron's subgenus Lygosoma) by having pterygoid teeth. The composition of the genus was greatly expanded by Boulenger (1887)in his influential classification of the lizards. In this classification, Leiolopisma (as Liolepisma), was a large 'section' of the redefined genus Lygosoma, which included all of the normally proportioned skinks combining a closed secondary palate with a transparent disc in the lower eyelid and lacking supranasal scales, a total of 50 species. Subsequent workers (notably Smith 1937; Mittleman 1952; Greer 1974) have restricted and refined the genus, but it has remained a grade group, whose members are identified by the absence of the synapomorphies diagnosing 0004-959X/90/050535$03.00
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other genera. Leiolopisma (sensu Greer 1974) is a member of the Eugongylus group (Greer 1979), a monophyletic assemblage of genera within which species of Leiolopisma are identified by the retention of a lacertiform habitus and a normal complement of head shields, by the presence of a transparent palpebral disc, and by the lack of the apomorphies which diagnose other genera. Important among these are: (1) the palatal structure (Greer & Parker 1968), which is of the alpha (pterygoids with smoothly diverging medial margins) rather than the beta type (pterygoids with posteromedial palatal processes); (2) a movable rather than fixed ('ablepharine'; Greer 1974) lower eyelid; (3) the retention of certain head shields (e.g, prefrontals, interparietal) lost or fused in other genera. Greer (1982) reviewed the Australian species, using the concept of Leiolopisma established in his earlier work (Greer 1974). Recent revisions of Leiolopisma species in two of their centres of diversity, New Zealand and New Caledonia, have resulted in further reduction in the size of the genus, by the recognition of Cyclodina in New Zealand (Hardy 1977) and several genera in New Caledonia (Sadlier 1986). In both cases, as in Australia, some species remain in Leiolopisma, identified by their grade of organisation rather than by synapomorphies. Zug (1985), describing L. alazon from Fiji, commented that the distribution of the species of Leiolopisma made 'little zoogeographic sense', and anticipated that future subdivisions of the genus would be needed. Since 1974, the number of Australian species has almost doubled, due to the discovery of new species or the resurrection of synonyms (see below), but relationships among them remain unresolved. Greer (1974) regarded Pseudemoia (sensu Rawlinson 1974) as synonymous with Leiolopisma, downgrading the significance of the one (plesiomorphic) feature, distinct supranasals, which distinguished its two included species, palfreymani and spenceri, from Leiolopisma. Pseudemoia has, however, continued to be recognised by subsequent workers (e.g. Brown 1987; Cogger et al. 1983; Rawlinson 1975; Rounsevell et al. 1985). Rawlinson (1975) and Greer (1982) have suggested that two lineages, the small-scaled, scansorial spenceri group and the larger-scaled, terrestrial baudini group, can be recognised in the Australian fauna, but the phylogenetic validity of these lineages has been questioned (Hutchinson et al. 1988; Shea 1987). The lineages proposed by Rawlinson and Greer are as follows: Leiolopisrna baudini group L. baudini Greer, 1982 L. entrecasteauxii (Dumeril & Bibron, 1839) L. rawlinsoni Hutchinson & Donnellan, 1988 L. duperreyi (Gray, 1838) L. platynoturn (Peters, 1881) L. trilineaturn (Gray, 1838) L. coventryi Rawlinson, 1975 L. metallicurn (O'Shaugnessy, 1874) L. zia Ingram & Ehmann, 1981 Leiolopisma spenceri group L. greeni Rawlinson, 1975 L. rnicrolepidoturn (O'Shaughnessy, 1874) L. ocellaturn (Gray, 1845) L. orocrypturn Hutchinson, Schwaner & Medlock, 1988 L. pretiosurn (O'Shaughnessy, 1874) L. (=Pseudernoia) palfreymani (Rawlinson, 1974) L. (=Pseudernoia) spenceri (Lucas & Frost, 1894) L. jigurru Covacevich, 1984
The present lack of a consensus on the phylogenetic relationships of these lizards is undoubtedly due to the conservative and convergent nature of morphological change within this group. The largely divergent nature of macromolecular sequence evolution means that molecular comparisons can often provide an independent source of data by which problematic patterns of morphological change can be understood. In order to obtain a new
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perspective on relationships within Leiolopisma we have made comparisons of the variation in sequence difference within the protein serum albumin, using the quantitative immunological technique of micro-complement fixation (MC'F) (Champion et al. 1974; Maxson & Maxson 1986). These comparisons, expressed as immunological distances, have enabled us to test existing hypotheses concerning the relationships among the Australian species assigned to Leiolopisma. Questions which we aimed to resolve included: Do the biochemical data support the notion of Leiolopisma as a single, monophyletic group? If not, how are the species related to other Australian genera? Do groups recognised immunologically have morphological features in common? Is it possible to develop an alternative generic arrangement to reflect these findings? Materials and Methods Micro-complement Fixation Serum albumin was purified by single-step polyacrylamide gel electrophoresis, the albumin being made visible with ANS (8-anilino-1-naphthalenesulphate,Mg salt) under ultra-violet light. Rabbits (IMVS coloureds: Hutchinson & Maxson 1986) were immunized over a 12-week period by standard procedures (Champion et ai. 1974). Purity of antisera was tested by immunoelectrophoresis, the presence of a single precipitin arc indicating an antiserum directed to a single plasma protein. MC'F experiments were carried out by the method of Champion et al. (1974), and the results of MC'F comparisons were expressed as units of immunological distance (ID). Antisera were raised to albumin purified from the following species: Leiolopisma duperreyi (Penola, S.A.); L. entrecasfeauxii (Lake Corangamite area, Vic.; these specimens represent the group 2 species of Donnellan & Hutchinson 1990); L. palfreymani (Pedra Branca islet, southern Tasmania); L. pretiosum (Albatross I., Bass Strait); Lampropholis guichenoti (Sydney, N.S.W.); La. challengeri (Sydney, N.S.W.); Morethia adelaidensis (Adelaide area, S.A.); Emoia longicauda (Papua New Guinea). In preliminary experiments, the last-named species proved to be distant from all of the Australian Leiolopisma and was used as the outgroup to root the phylogenetic tree. Details concerning sources of plasma samples and repositories of voucher specimens are provided in Appendix I. Cross-reactions using these antisera were carried out to produce a reciprocal matrix of ID values, and one-way comparisons were made t o most of the Australian Leiolopisma species (only L. baudini, L. rawlinsoni and L. trilineatum were unavailable), as well as a variety of other skink species. As all of the Australian species of Leiolopisma tested produced low ID values with at least one of the Leiolopisma antisera, no one-way comparisons with the Emoia antiserum were necessary. The reciprocal ID matrix was corrected for reciprocity by the method suggested by Cronin and Sarich (1975), with the added modification that the final correction factors were scaled to have a mean of 1.00. One-way distances were also scaled with these correction factors. The corrected reciprocals were averaged, and the resulting data analysed phylogenetically by the Fitch-Margoliash method (Fitch & Margoliash 1967), with the FITCH algorithm from PHYLIP version 3 . 1 (kindly supplied by Dr Joe Felsenstein). The Fitch-Margoliash method is preferred (over, e.g., various Wagner tree algorithms) for analysing distance data of the sort yielded by MC'F because it does not assume constant rates of evolution and it allows distances on the tree (output distances) to be less than measured (input) distances. Robustness of the tree was tested by jacknifing, following the suggestion of Lanyon (1985). Morphology External morphological data were obtained from specimens in the collection of the Museum of Victoria, and osteological data were obtained from osteological collections at La Trobe University, with additional data from some NMV and QM material (Appendix 1). Apomorphic character states were determined by outgroup comparison, with outgroups identified after the MC'F analysis. It is important to note, therefore, that the morphological data do not provide independent tests of the MC'F-based phylogeny; rather, they provide corroborative data and permit the diagnosis of taxa. Successive outgroup taxa used were non-Australian Eugongylus-group skinks, especially Eugongylus, Emoia, and the New Caledonian and New Zealand taxa, other normally proportioned lygosomines, such as Sphenomorphus (sensu lato), Mabuya and Egernia, and other normally proportioned skinks, particularly Eumeces.
Results The antiserum titres (incubation 23 h) ranged between 1/1800 and 1/3500. Table 1 shows the reciprocal matrix of ID values corrected for non-random reciprocity failure, along with the correction factor used. The raw data show a 12.2% standard deviation from perfect
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Table 1. Scaled reciprocal immunological distance values among eight species of Eugongylus-group skinks Data scaled by multiplying the columns of the raw data matrix by the correction factors shown. Standard deviations from reciprocity of corrected data is 6.4% Antigens
Leiolopisma duperreyi (DU) L. entrecasteauxii (EN)
L. palfreymani (PA) L. prefiosum (PR) Lampropholis guichenofi (GU) La. challengeri (CH) Morethia adelaidensis (MO) Emoia longicauda (EM) Correction factor
DU
EN
PA
Antisera PR GU
CH
MO
EM
0 31 39 41 51 45 32 65
30 0 19 20 33 34 32 45
39 22 0 6 15 16 45 40
39 24 6 0 14 16 41 42
61 29 18 16 15 0 52 53
28 33 55 38 41 57 0 70
58 48 33 49 56 55 66 0
1.12
1.14
0.97
1.12
44 31 14 13 0 15 54 53 0.87
0.92
1.27
0.81
reciprocity (Maxson & Wilson 1975), and the corrected data show a standard deviation of 6.4%. These values indicate that much of the apparent reciprocity failure was due to antiserum effects (individual sera giving consistently higher or lower ID values), and that the reciprocal ID values are in generally very close agreement. The best-fit Fitch-Margoliash tree found by means of PHYLIP is shown in Fig. 1. This tree has a standard deviation for goodness-of-fit (Fitch & Margoliash 1967) of only 5.1%, suggesting that the input data was distorted very little in the construction of the tree. Following Lanyon (1985), the data in Table 1 were jacknifed by dropping one taxon at a time and deriving the best-fit Fitch-Margoliash tree for the remaining seven taxa. This yielded a total of eight trees. All eight trees had exactly the same tree topology as Fig. 1, attesting to the robustness of the data. 6 7
-
I
14
Morethia adelaidensis Leiolopisrna duperreyi
Leiolopisrna pretiosurn Larnpropholis guichenoti 9
L
16
I
11
2 Leiolopisrna palfreyrnani
*
-
Leiolopisrna entrecasteauxii
-33-P
Larnpropholis challengeri Ernoia longicauda
Fig. 1. Fitch-Margoliash phylogenetic tree based on the scaled reciprocal I D values. Branch lengths show the proposed amount of albumin change along each branch. Goodness-of-fit, 5.1%.
The tree shows the species of Leiolopisma scattered through the group studied. The greatest divergence is between the Tasmanian endemics (L. palfreymani and L. pretiosum) and L. duperreyi, separated by average ID of 40. The Tasmanian species are more closely related to Lampropholis than to other Leiolopisma, and L. duperreyi is likewise closest to Morethia. Leiolopisma entrecasteauxii appears intermediate between these two groups, but the Fitch-Margoliash analysis consistently places it closer to the L, duperreyi-Morethia clade. The two species-groups within Lampropholis are represented by the antisera to La. challengeri and La. guichenoti; the two appear to be sister taxa. The range of variation within Australian Leiolopisma is emphasised by the fact that the outgroup genus, Emoia, is scarcely more distant than some Leiolopisma species are from each other. The branch lengths of the tree suggest an uneven rate of albumin evolution within the group studied, from relatively slow in the Tasmanian species (palfreymani and pretiosum) to relatively rapid in the Morethia-L. duperreyi clade.
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Table 2. Scaled reciprocal ID values integrated with one-way ID values among Eugongylus-group species Correction factors shown in Table 1. - =Not done; species clearly closely related to one reference species were not extensively compared with other antisera. Emoia antiserum not used for one-way comparisons Antigens PA
PR
GU
Antisera CH
EN
DU
MO
Leiolopisma greeni L. rnetallicum L. microlepidotum L. ocellatum L. orocryptum L. palfreymani (PA) L. pretiosum (PR) L. coventryi L. jigurru L. zia 'Nannoscincus' maccoyi Lampropholis quichenoti (GU) La. challengeri (CH) Pseudemoia spenceri L. 'entrecasteauxii' gp 1 L. 'entrecasteauxii' gp 2 (EN) L . duperreyi (DU) L. platynotum Morethia adelaidensis (MO) M. boulengeri M. lineoocellata M. obscura M. taeniopleura L. grande Cyclodina oliveri L. lichenigerum L. nigrofasciolaturn Caledonescincus austrocaledonicus L. telfairii Eugongylus rufescens
One-way comparisons are shown in Table 2. The scaling factors shown for each antiserum in Table 1 have been applied to these data to make the columns as comparable as possible. In determining the probable branching points for these species it is important to note the rank-order of species within columns, as well as the absolute values of the ID measurements. Relationships of species can be best estimated if they show a significantly lower ID to one antiserum. Many of the species gave ID values to all antisera in the range of 25-40, and cannot be certainly placed in the absence of reciprocal comparisons. This table confirms the disparate nature of species currently included in Leiolopisma, because several clusters can be recognised. The endemic Tasmanian species, L. greeni, L. microlepidotum,L. ocellatum, L. orocryptum, L. palfreymani and L. pretiosum, plus L. metallicum, are all extremely closely related. Pseudemoia spenceri is similarly close to L. entrecasteauxii. Leiolopisma coventryi, L. jigurru and L. zia are intermediate between the Tasmanian group and Lampropholis, if anything being closer to the former than to the latter lineage. The data do not of course show whether any of these three species are closer to one another than to the Tasmanian group or Lampropholis. Leiolopismaplatynotum is rather distantly related to most other Leiolopisma, apart from L. duperreyi. Morethia taeniopleura, a member of a distinct, northern species-group (Greer
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1980) within Morethia, is very closely related to M. adelaidensis, which belongs to the morphologically different southern species-group (Greer 1980). Thus the Australian species of Leiolopisma belong to at least four distinct lineages: (1) the Tasmanian species; (2) the trio of species (L. coventryi, L. jigurru and L. zia) intermediate between this group and Lampropholis; (3) Pseudemoia plus L. entrecasteauxii; (4) Morethia plus L. duperreyi. The Australian species-clusters in Leiolopisma are each closer to other Australian genera then they are to any of the non-Australian species, L. grande (New Zealand), L. lichenigerum (Lord Howe I.), L. nigrofasciolatum (New Caledonia) and L , telfairii (Mauritius). Each of the extralimital Leiolopisma is about as distinct from the Tasmanian Leiolopisma as it is from L. duperreyi, indicating that all may have diverged from the Australian assemblage at the same time as the latter was beginning its diversification. A possible exception is the consistently relatively low ID values obtained to the extralimital species with the L. entrecasteauxii antiserum. However, the short branch-length to this species in Fig. 1 implies a relatively slow rate of change for its albumin, making it difficult to interpret somewhat lower ID values as positive evidence for close relationship. Crossreactions to L , telfairii revealed no obvious sister-group relationship with any of the Australian species-clusters. The relationships of L. telfairii to the New Zealand and New Caledonian species are not resolved by this data set; such a resolution will require antisera representing at least two of the relevant geographic groups.
Discussion
Generic Revision of Leiolopisma in Australia The results of the MC'F comparisons suggest that Leiolopisma as currently diagnosed is polyphyletic, including several long-separated evolutionary lineages. Continued recognition of Leiolopisma as a strictly monophyletic genus would not be justified on the basis of these results. Given this, do the other recent suggestions concerning relationships within Leiolopisma find any support? Certainly, the MC'F data d o not support the large-scaled v. small-scaled dichotomy within Leiolopisma (Greer 1982; Rawlinson 1974, 1975; p. 536). In addition, Rawlinson's (1974) concept of Pseudemoia is not supported. However, the clades delineated by the immunological comparisons can be corroborated by morphological data. We regard these clades as genera, which are defined and discussed further below. Features found to be useful in diagnosing monophyletic groups include: frontoparietal shields paired or single (Fig. 2); width of rostral-frontonasal contact (Fig. 2); size and shape of the palpebral disc (Fig. 3); configuration of the bones of the palate (Fig. 4); degree of closure of the upper temporal fenestra (Fig. 5); number of presacral vertebrae; mode of reproduction; presence or absence of heteromorphic sex chromosomes; presence or absence of bright ventral pigmentation or sexual dichromatism. The polarity of the states of these characters is outlined in Appendix 11. All of the following genera are members of the Eugongylus group (Greer 1979) of the subfamily Lygosominae and possess the following suite of character states: single frontal bone (synapomorphy for Lygosominae); 11 premaxillary teeth; postorbital bone absent; groove for meckelian cartilage completely overgrown by dentary; pterygoid teeth absent; parietal shields contact behind the interparietal; parietals contacted posterolaterally by the upper secondary temporal and an enlarged nuchal; a single row of supradigital scales (synapomorphies for Eugongylus group). All species have a diploid chromosome number of 30. Other character states plesiomorphic for the following group of genera are: frontoparietal shields paired, interparietal large; rostral-frontonasal suture narrow to moderate; palpebral disc elongate-oval, length 50% or less that that of eye; upper temporal fenestra present, narrowly elliptical in shape; fewer than 30 presacral vertebrae; alpha palate; nasal-premaxillary suture narrow, V-shaped; males without heteromorphic pair seven sex chromosomes; oviparity. Generic diagnoses are given only in terms of synapomorphies.
Generic Revision of Leiolopisma
Fig. 2. Headshield arrangements of: (a) Pseudemoia entecasteauxii group 2 (King I., NMV D62219), showing paired frontoparietals (fp), relatively narrow contact between the rostra1 (r) and frontonasal (fn), and normally proportioned supraciliaries (sc, longer than wide in dorsal view); (b) Niveoscincus metallicus (Western Arthur Range, Tas., LTU unregistered), with single frontoparietal (fp), moderate interparietal (ip) and narrow rostral-frontonasal suture; (c) Cautula zia, with frontoparietals paired and the rostral-frontonasal suture broad; (d) Bassiana trilineata (Eyre Pen., S.A., NMV D60955), with frontoparietal single, the interparietal small and the rostral-frontonasal suture moderate; (e) Bartleia jigurru, with paired frontoparietals, moderate rostral-frontonasal suture and transversely enlarged supraciliaries. 2(c) Redrawn from Ingram and Ehmann (1981, fig. 1); (e) redrawn from Covacevich (1984, pl. 2b). Magnification x 6.
Fig. 3. Palpebral discs of: (a) Niveoscincus pretiosus (Mt Wellington, Tas., TMH C582; moderate size, elongate oval shape); (b) Pseudemoia spenceri (Gunmark Rocks, East Gippsland, Vic., NMV D48568; large, almost circular). Also shown is the fused supranasal+postnasal scale typical of P. spenceri. Magnification x 10.
M. N. Hutchinson et al.
Fig. 4. (a) Palatal view o f skull o f Pseudemoia entrecasteauxii group 1 (Avalon, Vic., LTU 86/23). (b)-( f ) Palatal complexes o f : (b) P. spenceri (Mt Baw Baw, Vic., LTU 86/30); (c) Niveoscincus metallicus (Bayles, Vic., LTU 85/52); ( d ) N. ocellarus (Hamilton, Tas., 85/55); (e) Bassiana irilineata (East Mt Barron, W . A . , 85/59); ( f ) Cauiula zia (Wiangarie State Forest, N.S.W., 86/32). Note variation in the shape o f the bones o f the secondary palate, the palatines ( p l ) and pterygoids (pg). Magnification x 6.
Genus Bassiana, gen, nov. Eulepis Fitzinger, 1843, p. 22. [Not Eulepis Dalmann MS, in Billberg (1820); Lepidoptera.] Bassiana, nom. nov. pro Eulepis Fitzinger, 1843.
Type-species: Lygosoma duperreyi Gray, 1838. Diagnosis. Eugongylus-group skinks with 'frontoparietals fused to form a single shield, interparietal reduced; supranasals absent; rostral-frontonasal suture almost as wide as frontal; limbs relatively short, typically just touching when adpressed in males, but failing to contact in females; breeding males with red throat colouration; heteromorphic sex chromosomes present; 29-34 presacral vertebrae; upper temporal fenestra absent. Included species. Tiliqua duperreyi Gray, 1838; Lygosoma (Mocoa) platynotum Peters, 1881; Tiliqua trilineata Gray, 1838. Etymology. From the Bassian zoogeographic subregion, the boundaries of which are coincident with the collective distributions of the three included species. Genus feminine. Distribution. Temperate southern Australia and Tasmania, with a south-western species (trilineata), a south-eastern species (duperreyi) and an eastern species (platynotum).
Generic Revision of Leiolopisma
Fig. 5. Dorsal view of skull of: (a) Niveoscincus microlepidotus (Mt Wellington, Tas., LTU 86/2), showing moderate supratemporal fenestra (stf) and V-shaped suture between the nasal (n) and premaxillary (pmx) bones; (b) Cautula zia (Wiangerie State Forest, N.S.W., LTU 86/32), showing loss of supratemporal fenestra and W-shaped nasal-premaxillary suture. Magnification x 7.
Comments. The two species in this complex available for testing are closely related biochemically, and are distant from the other Australian species included in Leiolopisma. They share a close relationship with Morethia, as suggested by Greer (1980). Bassiana shares a unique combination of synapomorphies with Morethia, namely the universal presence of the male pair 7 X Y sex-chromosome system (Donnellan 1985), red breeding colour in males, elevated presacral count, fused frontoparietals and virtual or complete closure of the upper temporal fenestra, all of which tend to support the immunological data. This same suite of derived character states is also mostly shared with Pseudemoia (below), apart from the latter's retention of paired frontoparietals.
Genus Pseudemoia Fuhn Pseudemoia Fuhn, 1967, p. 73.
Type-species: Lygosoma (Emoa) spenceri Lucas & Frost, 1894, by original designation. Diagnosis. Eugongylus-group skinks with a large, almost circular palpebral disc (diameter >50% of eye diameter) in a movable lower eyelid; breeding males with areas of red pigmentation (absent in P. spenceri and P. rawlinsoni); heteromorphic sex chromosomes present; palatal rami of the pterygoids (except in some P, rawlinsoni) with moderate to well developed angular expansions, with beta-like posteromedial processes in some species; 28-31 presacral vertebrae; upper temporal fenestra absent; viviparous. Included species. Leiolopisrna baudini Greer, 1982; Gongylus (Lygosoma) entrecasteauxii Dumtril & Bibron, 1839 (groups 1 and 2 of Donnellan & Hutchinson 1990); Leiolopisma rawlinsoni Hutchinson & Donnellan, 1988; Lygosoma (Emoa) spenceri Lucas & Frost, 1894. Distribution. Temperate south-eastern Australia and Tasmania, from the New England Tableland to Tasmania and west to the Great Australian Bight coast. Occurs from sea level to the highest alpine elevations, but absent from the warm temperate eastern Victorian and New South Wales coasts.
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Comments. The species in this genus are very closely related, scarcely distingishable by albumin MC'F. Pseudemoia does not show a sister-group relationship with any of the other species formerly included in Leiolopisma, although it shares a common ancestry with Bassiana and Morethia. Pseudemoia also cuts across the traditional subgroups within the Australian members of the genus (Greer 1982; Rawlinson 1974) in that it includes a smallscaled climber (the type-species of Pseudemoia, P . spenceri) and as many as five (Donnellan & Hutchinson 1990) larger-scaled terrestrial forms making up the L. baudini species-complex (Hutchinson & Donnellan 1988). The genus retains some plesiomorphies (paired frontoparietals, supranasals in some species), but its species have several synapomorphies, notably an unusually large subcircular palpebral disc (so large that museum workers unfamiliar with the live animals considered P. spenceri to have an immovable lower eyelid, e.g. Smith 1935; Greer 1974), the modification of the alpha palate by the development of pterygoid angularities or beta-palate-like processes (Hutchinson & Donnellan 1988) and viviparity with an advanced chorioallantoic placenta (Harrison and Weekes 1925). As noted earlier, several derived character states ally this genus with Bassiana and Morethia, and strongly support the immunological finding that these genera constitute a distinct phylogenetic group within the Eugongylus group.
Genus Niveoscincus, gen. nov. Type-species: Leiolopisma greeni Rawlinson, 1975. Diagnosis. Eugongylus-group skinks with frontoparietals fused to form a single shield (paired in N. coventryi); supranasals absent (present in N. palfreymani); body shape variable interspecifically, some species showing marked dorso-ventral flattening; viviparous. Included species. Leiolopisma coventryi Rawlinson, 1975; Leiolopisma greeni Rawlinson, 1975; Mocoa metallica O'Shaughnessy, 1874; Mocoa microlepidota O'Shaughnessy, 1874; Mocoa ocellata Gray, 1845; Leiolopisma orocryptum Hutchinson, Schwaner & Medlock, 1988; Pseudemoia palfreymani Rawlinson, 1974; Mocoa pretiosa O'Shaughnessy, 1874. Etymology. From the latin nivea, snow, and neo-Latin scincus, a skink, alluding to the cold climates inhabited by these skinks. Genus masculine. Distribution. Primarily Tasmanian, with one species (N. metallicus) shared with southern Victoria, and one (N, coventryi) confined to cool temperate montane forests in Victoria and south-eastern New South Wales. Comments. The Tasmanian species form another very tight cluster with the molecular data supporting the proposal (Hutchinson et al. 1988) that the Tasmanian L. spenceri-group species are closely related to each other and closer to L. metallicum than to L. spenceri. The data thus also suggest that 'Pseudemoia' palfreymani is much more closely related to the Tasmanian Leiolopisma species, and in turn to some other Eugongylus-group genera, than it is to P. spenceri. As with our revised Pseudemoia, Niveoscincus consists of a mixture of small-scaled climbers (most species) and large-scaled strictly terrestrial species (N. coventryi and N. metallicus). Niveoscincus species are also all viviparous, but are derived with respect to Pseudemoia in that, with the exception of N. coventryi, the frontoparietal shields are fused. In other respects, Niveoscincus is plesiomorphic, retaining the normal alpha palate configuration, a moderate, oval palpebral disc and (except for N. coventryi) a moderate upper temporal fenestra. The species in this genus also, as far as is known (data available for all but N. coventryi and N. orocryptus), lack heteromorphic sex chromosomes. Leiolopisma coventryi Rawlinson, 1975, is included in this genus with some reservation. It is immunologically close to the Tasmanian species although, at the present state of knowledge, no more so than two other distinctive species of Leiolopisma, jigurru and zia. Leiolopisma coventryi is relatively unspecialised morphologically but has evolved viviparity.
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This is known in only two Australian Eugongylus-group lineages, the Tasmanian group and Pseudemoia. Leiolopisma coventryi is phylogenetically close to the former group and it seems conservative to attribute viviparity in these two as due to shared common ancestry. Leiolopisma coventryi lacks the fused frontoparietals characteristic of the Tasmanian group, and has the apomorphic state (loss) of the upper temporal opening. In other respects L. coventryi is very similar to the Tasmanian species, and can be regarded as their sisterspecies. This relationship could be expressed either by monotypic generic status or by inclusion in a genus together with the Tasmanian species. Since viviparity is a derived state which appears to indicate a particular relationship for L. coventryi, we prefer to take the latter option, but future studies should bear in mind that our generic placement is provisional. Genus Cautula, gen, nov. Type-species: Leiolopisma zia Ingram & Ehmann, 1981. Diagnosis. Eugongylus-group skinks with supranasals absent; rostral-frontonasal suture broader than frontal; limbs short, fail to contact when adpressed; belly of both sexes bright yellow in life; 31-32 presacral vertebrae; broad, W-shaped nasal-premaxillary suture; upper temporal fenestra absent. Included species. Monotypic; Leiolopisma zia Engram & Ehmann, 1981. Etymology. From the Latin cauta, shy, and the diminutive suffix -ula, alluding to the small size and secretive habits of the type-species. Genus feminine. Distribution. Queensland.
Mountain forest areas of north-eastern New South Wales and far southern
Comments. As with N. coventryi, C. zia is distinct morphologically, but of uncertain relationships because of the lack of specific antisera. Ingram & Ehmann (1981) saw some similarity between C, zia and N. coventryi in colour pattern, and the two are similar in being ecological equivalents, both being confined to cool to cold wet sclerophyll-Nothofagus forests, N. coventryi in the south-east mainland and C. zia in the New England area (north-eastern New South Wales). Other data, however, do not suggest an especially close relationship between them. C. zia retains oviparity, but differs from L. coventryi in having five apomorphic character states: a broad, W-shaped suture between the premaxillae and nasals, a reduced ear opening, increased presacral vertebral number, bright yellow ventral colouring, and short, non-overlapping limbs. Possible sister-groups of this species include Lampropholis and 'Nannoscincus' maccoyi. Lampropholis shares a broad and often W-shaped nasal-premaxillary suture, and the L. challengeri group includes species which are cryptic in habits, as is C. zia. However, Lampropholis species have a well developed beta palate and show no limb reduction, apart from digital loss on the forelimb of La. tetradactyla and shorter limbs in La, caligula. 'Nannoscincus' maccoyi in not certainly congeneric with true Nannoscincus from New Caledonia, and is an attenuate litter swimmer which shares with C. zia the W-shaped nasal-premaxillary suture, increased presacral count, and yellow belly. It is more specialised than C. zia, with even more reduced limbs and ear opening, and loss of prefrontal shields, associated with a shortened, pointed snout. The one-way ID'S indicate that maccoyi reacts similarly to zia, but we lack direct immunological evidence for a sister-group relationship between the two. The evidence suggests that although zia may be closely related to Lampropholis it has a unique combination of derived character states and lacks the beta palate. Though a closer relationship to 'N.' maccoyi seems more likely, the uncertain generic position of the latter requires a study of its own, and we have no direct biochemical evidence bearing on this possible relationship. We suggest that the presence of a distinctive array of apomorphic character states requires separate generic status for C. zia, but future studies may result in the expansion of this genus to include 'N.' maccoyi.
M. N. Hutchinson et al.
Genus Bartleia, gen, nov. Type-species: Leiolopisma jigurru Covacevich, 1984. Diagnosis. Pentadactyle Eugongylus group skinks with supranasals absent; supraciliaries enlarged, as wide as long in dorsal view; head and body flattened; nasal processes of premaxillaries broadened; upper temporal fenestra closed. Included species. Monotypic; Leiolopisma jigurru Covacevich, 1984. Etymology. The name is based on Mt Bartle Frere, the only known habitat of the species. Genus feminine. Distribution. Confined to the summit of Mt Bartle Frere in north-east Queensland. Comments. Bartleia jigurru has a distinctive combination of plesiomorphic and apomorphic character states and is geographically remote from the other Australian species formerly in Leiolopisma, being restricted to the summit of Mt Bartle Frere in north-eastern Queensland, a cloud-forest environment in which the species is confined to granite boulders (Covacevich 1984). Immunologically, the species shares the intermediate position (between Lampropholis and Niveoscincus) of N. coventryi and C. zia. In addition, the combination in jigurru of a closed upper temporal fenestra, noticeably broadened nasal processes of the premaxillae, and loss of supranasals, collectively occurs also in Lampropholis, 'N.' maccoyi and C. zia, and further supports its sharing of a common ancestry with these taxa. More direct biochemical evidence, in the form of an antiserum to B. jigurru albumin or electrophoretic data, would be helpful in clarifying its relationships, pending which its generic position is unclear. It could be retained in Leiolopisma until its relationships are better known, although it is obviously not related to L. telfairii. It could be included in one of the closely related genera noted above, although this would not be supported by any synapomorphies. The third choice, separate generic status, seems the most useful, in that it draws attention to the species' lack of an obvious sister-species while affirming that, at least, it is not a close relative of L. telfairii. Relationships of Leiolopisma telfairii Leiolopisma telfairii does not share an obvious sister-group relationship with any of the Australian Eugongylus-group species for which antisera were available. However, the MC'F comparisons (including work in preparation) do support the close relationship of this species to the Australian Eugongylus-group radiation, and are backed up by some significant morphological similarities. Some of this discussion draws on Greer's (1976) comments on the extinct Didosaurus mauritianus, a giant Mascarene species known from subfossil skeletal remains. Arnold (1980) has shown that this species is indistinguishable except in size from L. telfairii (with which it was contemporaneous), and has synonymised Didosaurus with Leiolopisma. L. telfairii and L. rnauritianum have 11 premaxillary teeth, an increase over the 9 usually present in lygosomines (Neotropical Mabuya may also have 11) and a diagnostic feature for the Eugongylus group. Both species also have an alpha palate with posteromedial processes on the trailing edges of the palatines, always present in Eugongylus-group genera but often absent in other skinks with apposed palatines. Leiolopisma telfairii has 28 presacral vertebrae (based on a single NMV specimen), and since it is a long-limbed, non-attenuate species, this also indicates membership in the Eugongylus group (other normally proportioned skinks have 26 presacrals). Hardy (1979) has reported that L, telfairii has a diploid chromosome number of 30, with a similar arrangement of chromosomal sizes to that seen in other Eugongylus-group taxa (Donnellan 1985). The single male karyotyped by Hardy showed no chromosome heteromorphism, although the quality of the preparations was poor. Leiolopisma telfairii and L. mauritianum differ from the Australasian members of the Eugongylus group in that they retain pterygoid teeth (Dumkril& Bibron 1839; Arnold 1980). Loss of this character state was one of the synapomorphies used by Greer (1979) to define
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the Eugongylus group. Greer, like other workers post-Boulenger, has treated Leiolopisma as being composed only of species lacking pterygoid teeth, in spite of the presence of such teeth in the type-species of the genus. No doubt a contributing factor for this treatment is the variable presence or absence of pterygoid teeth in L. telfairii, a fact not noticed until the study by Arnold (1980). It is one of the curious features of the history of this generic name that no taxonomist has been struck by the contradiction in this respect between DumCril and Bibron's diagnosis of the type-species of Leiolopisma and subsequent redefinitions of this genus. Had this happened, Leiolopisma may well have been restricted a t an early stage to the peculiar island endemic for which it was first erected. Other features which appear to be unique and are probably autapomorphies involve cephalic scalation. The first three of the four supraocular scales contact the frontal in L. telfairii, rather than only the first two as in the other Eugongylus-group taxa. In addition, L. telfairii has a unique parietal and temporal scalation, with large parietals which have an angular posterolateral corner and which contact numerous small nuchal scales posteriorly and up to three small temporal scales laterally. None of the other Eugongylus group genera show any trends towards this distinctive scalation. In summary, it appears that L. telfairii shares a common ancestry with the Australian Eugongylus-group species, including those traditionally placed in Leiolopisma, but the MC'F data and its morphological peculiarities imply that it forms a lineage of its own, not sharing a recent common ancestry with any of the Australian Eugongylus-group taxa regarded in the past as congeneric. This separate evolutionary history would best be reflected by restricting the content of Leiolopisma to a single living species, L. telfairii, and the extinct L, mauritianum.
Relationships of Other Non-Australian Leiolopisma Although we have not yet carried out extensive comparisons among extra-limital 'Leiolopisma', we are confident that none is congeneric with any of the Australian taxa. Preliminary MC'F data suggest that both the New Caledonian and New Zealand-Lord Howe I. species remaining in 'Leiolopisma' are likely to be part of the Australian regional Eugongylus-group radiation, but neither is close to any particular Australian lineage, and each appears to be no closer to the other than to the Australian genera (unpublished data). The New Caledonian species left in Leiolopisma include two rather distinct morphological types (Sadlier 1986): slender, arboreal species (greeri, nigrofasciolatum and novaecaledoniae) and a dumpier, short-snouted form (steindachneri). Lioscincus Bocage, 1873, is available for the latter species, but a new genus may be required for the first three. In the New Zealand fauna, Oligosoma Girard, 1857, could be revived for the species not placed in Cyclodina by Hardy (1977). The Fijian endemic, L. alazon, is probably close to one of the New Zealand genera (Zug 1985).
Evolutionary Patterns within the Eugongylus Group The relationships suggested by both the MC'F data, including one-way comparisons, and with the evidence from morphology are summarised in Fig. 6. The branching order of the tree in Fig. 1 has been retained, except that the very short (1 ID unit) branch separating the Tasmanian species has been collapsed, and these two species are placed as a monophyletic unit. Specifying this topology gives only a slightly worse fit of the data, increasing the percentage SD of the tree from 5.1% to 5.3%, and this sister-group relationship is supported by electrophoretic data (Hutchinson & Schwaner, in press) as well as the morphological data discussed in the generic descriptions. Species compared in one-way experiments have dashed lines to their estimated branching points, and generic groupings of the species formerly placed in Leiolopisma are shown. This study suggests a major change in out understanding of phylogenetic relationships among the Australian Eugongylus-group taxa. The polyphyly of 'Leiolopisma' was suspected before our work began, but several rather long-held views concerning relationships among these skinks are called into question by our results.
M. N. Hutchinson et al. MORETHIA
7
duperreyi
BASSIANA
platynoturn spenceri
entrecasteauxii Cp 2
guichenoti LAMPROPHOLIS chailengerl 'W." maccoyi ria jigurru
CAU7'ULA
7 BARTLEIA
palfreymani pretiosus green1 meralllcus microlepidotus ocella tus orocryptus
NiVEOSCINCUS
New Zealand species New Caledonian specles
Fig. 6. Tree essentially retaining the branching order shown in Fig. 1, modified by the addition of species examined in one-way comparisons, shown as dashed lines. Composition of the new genera proposed is indicated by square brackets, with dashed outlines where membership in a genus is uncertain.
Rawlinson (1974, 1975) and Greer (1982) found that midbody scale size correlated with some other features (litter size, proportions of limbs), suggesting two phyletic groups, the larger-scaled L. baudini group and the smaller-scaled L. spenceri group. Our data suggest that although the two groups may predict ecology (scansorial spenceri group versus nonclimbing, litter-dwelling baudini group), they do not indicate phylogenetic relationships. Within the L. baudini group, for instance, are two of the most distantly related Eugongylusgroup taxa, Bassiana and Niveoscincus. At the other extreme, there are L. spenceri-group species which are very close relatives of L. baudini-group species (e.g. Niveoscincuspretiosus and N. metallicus). The evolution of the flattened head and body, the long, sprawling limbs and the soft, small-scaled skin in the L. spenceri group all appear to be adaptations to improve locomotion over vertical surfaces and concealment in cracks and crevices. This morphological trend is evident in several Eugongylus-group genera, including Pseudemoia, Niveoscincus, Lampropholis, Lygisaurus and Carlia (noted also by Covacevich & Ingram 1978; Ingram & Covacevich 1988). Arnold (1973) has noted an analogous trend in European Lacerta, where the saxicoline species are flatter and longer limbed, and have softer skins, than do related non-climbing species. The MC'F study has indicated clusters of species which are definable and corroborated by non-biochemical data, giving us some confidence in the validity of the major genera proposed, i.e. Bassiana, Pseudemoia and Niveoscincus. However, three species, coventryi, zia and jigurru, are placed with less confidence. The three are relatively closely related to each other and to several other Eugongylus-group clades, including Lampropholis and the Tasmanian Niveoscincus, but the cladistics of these groups are not resolved by the MC'F
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data. We have therefore had to place these species on the basis of data of uncertain phylogenetic reliability, guided as much by evidence concerning taxa to which the species were not related, as by positive evidence for a particular generic placement. The relationships of all three species clearly need further study. Our partial survey of relationships among the Eugongylus-group genera suggests the existence of several independent adaptive radiations, each tending to follow a similar pattern of diversification characterised by frequent and detailed cases of parallel and convergent evolution. The Australian species formerly placed in Leiolopisma are derived from two such radiations, the first represented by Niveoscincus, Lampropholis and related taxa, the second by Pseudemoia, Bassiana and Morethia. The initial divergence of the Australian lineages hitherto included in Leiolopisma was apparently synchronous with that of the New Caledonian and New Zealand radiations and, in spite of the fact that superficial similarities have long placed these species in the same genus, the ID values obtained between some lineages represent about as great a degree of albumin divergence as is known in the Eugongylus group. Further studies are in progress to generate a more complete picture of the phylogenetic pattern linking the genera of the Eugongylus group.
Acknowledgments We thank the following colleagues for the provision of specimens or plasma samples; A. Allison, K. Aplin, N. Brothers, H. G. Cogger, J. Covacevich, C. H. Daugherty, G. Gowing, A. E. Greer, R. Jenkins, B. Miller, W. Osborne, R. Sadlier, G. Shea and T. D. Schwaner. We also thank J. Birrell for technical help. P. Couper and G. Ingram (QM) provided the osteological data on Bartleia jigurru, and H. G. Cogger helped with some nomenclatural problems. R. Sadlier critically read and improved an earlier draft of the manuscript. This work was supported by an ARGS grant to P. Baverstock and M. Adams, a CTEC special research grant to M. Hutchinson, and a Commonwealth Postgraduate Research Award to S. Burgin. We thank the state wildlife authorities of South Australia, Victoria, New South Wales, Queensland, Western Australia and Tasmania for permitting us to collect skink specimens, and the Australian Customs and Animal Quarantine Services for permission to import blood of exotic species. References Arnold, E. N. 1973. Relationships of the Palaearctic lizards assigned to the genera Lacerta, Algyroides and Psammodromus. Bulletin of the British Museum (Natural History), Zoology 25, 291-366. Arnold, E. N. 1980. Recently extinct reptile populations from Mauritius and Reunion, Indian Ocean. Journal of Zoology (London) 191, 33-47. Boulenger, G. A. 1887. 'Catalogue of the Reptiles in the British Museum (N.H.).' 111. (Taylor & Francis: London.) Brown, G. W. 1987. The diet of Pseudemoia spenceri (Lucas and Frost, 1894) (Lacertilia : Scincidae), a species endemic to south-eastern Australia. Victorian Naturalist 103, 48-55. Champion, A. B., E. M. Prager, D. Wachter & A. C. Wilson. 1974. Micro-complement fixation. Pp. 397-417 in: 'Biochemical and Immunological Taxonomy of Animals'. Ed. C. A. Wright. (Academic Press: London.) Cogger, H. G., E. E. Cameron & H. M. Cogger. 1983. 'Zoological Catalogue of Australia. I. Amphibia and Reptilia. (Australian Government Publishing Service: Canberra.) Covacevich, J. 1984. A biogeographically significant new species of Leiolopisma (Scincidae) from north eastern Queensland. Memoirs of the Queensland Museum 21, 401-11. Covacevich, J. & G. J. Ingram. 1978. An undescribed species of rock-dwelling Cryptoblepharus (Lacertilia : Scincidae). Memoirs of the Queensland Museum 18, 151-4. Cronin, J. E. & V. M. Sarich. 1975. Molecular systematics of the New World monkeys. Journal of Human Evolution 4, 357-75. Donnellan, S. C. 1985. The evolution of sex chromosomes in scincid lizards. Ph.D. Thesis, Macquarie University. Donnellan, S. C. & M. N. Hutchinson. 1990. Biochemical and morphological variation in the geographically widespread lizard Leiolopisma entrecasteauxii (Lacertilia : Scincidae). Herpetologica. 46, 149-59.
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DumCril, A. M. C. & G. Bibron. 1839. 'Erpetologie GCnCrale ou Histoire Naturelle Complkte des Reptiles.' V. (Roret: Paris.) Estes, R., K. de Queiroz & J. Gauthier. 1988. Phylogenetic relationships within Squamata. Pp. 119281 in: 'Phylogenetic Relationships of the Lizard Families'. Eds R. Estes & G. Pregill. (Stanford University Press: Stanford.) Fitch, W. M. & E. Margoliash. 1967. Construction of phylogenetic trees. Science (New York) 155, 279-84. Puhn, I. E. 1967. Pseudemoia, eine neue monotyische Gattung aus Siidostaustralien (Ablepharus/Emoa spenceri Lucas and Frost). Zoologische Anzeiger 179, 243-7. Greer, A. E. 1974. The generic relationships of the scincid lizard genus Leiolopisma and its relatives. Australian Journal of Zoology, Supplementary Series, No. 31, 67 pp. Greer, A. E. 1976. On the evolution of the giant Cape Verde scincid lizard Macroscincus coctei. Journal of Natural History 10, 691-712. Greer, A. E. 1979. A phylogenetic subdivision of Australian skinks. Records of the Australian Museum 32, 339-71. Greer, A. E. 1980. A new species of Morethia (Lacertilia : Scincidae) from northern Australia, with comments on the biology and relationships of the genus. Records of the Australian Museum 33, 89-122. Greer, A. E. 1982. A new species of Leiolopisma (Lacertilia : Scincidae) from Western Australia, with notes on the biology and relationships of other Australian species. Records of the Australian Museum 34, 549-73. Greer, A. E. & F. Parker. 1968. Geomyersia glabra, a new genus and species of scincid lizard from Bougainville, Solomon Islands, with comments on the relationships of some lygosomine genera. Breviora No. 302, 17 pp. Hardy, G. S. 1977. The New Zealand Scincidae (Reptilia : Lacertilia), a taxonomic and zoogeographic study. New Zealand Journal of Zoology 4, 221-325. Hardy, G. S. 1979. The karyotypes of two scincid lizards, and their bearing on relationships in genus Leiolopisma and its relatives (Scincidae : Lygosominae). New Zealand Journal of Zoology 6, 609- 12. Harrison, L. & H. C. Weekes. 1925. On the occurrence of placentation in the scincid lizard Lygosoma entrecasteauxii. Proceedings of the Linnean Society of New South Wales 50, 470-86. Hoffstetter, R. & J.-P. Gasc. 1969. Vertebrae and ribs of modern reptiles. Pp. 201-310 in: 'Biology of the Reptilia'. Eds C. Gans, A. d'A. Bellairs & T. S. Parsons. (Academic Press: New York and London.) Hikida, T . 1978. Postembryonic development of the skull of the Japanese skink Eumeces latiscutatus (Scincidae). Japanese Journal of Herpetology 7, 56-72. Hutchinson, M. N. & S. C. Donnellan. 1988. A new species of scincid lizard from southeastern Australia, related to Leiolopisma entrecasteauxii. Transactions of the Royal Society of South Australia 112, 143-51. Hutchinson, M. N. & L. R. Maxson. 1986. Immunological evidence on relationships among some Australian terrestrial frogs (Anura : Hylidae : Pelodryadinae). Australian Journal of Zoology 34, 575-82. Hutchinson, M. N. & T. D. Schwaner. In press. Genetic relationships among the Tasmanian scincid lizards of the genus Niveoscincus. Journal of Herpetology 25. Hutchinson, M. N., T . D. Schwaner & K. Medlock. 1988. A new species of scincid lizard from the highlands of southwest Tasmania. Proceedings of the Royal Society of Victoria 100, 67-73. Ingram, G. J. & J. Covacevich. 1988. Revision of the genus Lygisaurus de Vis (Scincidae : Reptilia) in Australia, Memoirs of the Queensland Museum 25, 335-54. Ingram, G. J. & H. Ehmann. 1981. A new species of scincid lizard of the genus Leiolopisma (Scincidae : Lygosominae) from south eastern Queensland and north eastern New South Wales. Memoirs of the Queensland Museum 20, 307-10. Lanyon, S. 1985. Detecting internal inconsistencies in distance data. Systematic Zoology 34, 397-403. Leviton, A. E., R. H. Gibbs Jr, E. Heal & C. E. Dawson. 1985. Standards in herpetology and ichthyology: Part I. Standard symbolic codes for institutional resource collections in herpetology and ichthyology. Copeia 1985, 802-32. Maxson, L. R. & A. C. Wilson. 1975. Albumin evolution and organismal evolution in tree frogs (Hylidae). Systematic Zoology 24, 1-15. Maxson, R. D.& L. R. Maxson. 1986. Micro-complement fixation: a quantitative estimator of protein evolution. Molecular Biology and Evolution 3, 375-88. Mittleman, M. B. 1952. A generic synopsis of the lizards of the subfamily Lygosominae. Smithsonian Miscellaneous Collections 117, 1-35. Pengilley, R. 1972. Systematic relationships and ecology of some lygosomine lizards from southeastern Australia. Ph.D. Thesis, Australian National University.
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Rawlinson, P. A. 1974. Revision of the endemic southeastern Australian lizard genus Pseudemoia (Scincidae : Lygosominae). Memoirs of the National Museum of Victoria 35, 87-96. Rawlinson, P. A. 1975. Two new lizard species from the genus Leiolopisma (Scincidae : Lygosominae) in southeastern Australia. Memoirs of the National Museum of Victoria 36, 1-16. Rounsevell, D., N. Brothers & N. Holdsworth. 1985. The status and ecology of the Pedra Branca skink, Pseudernoiapalfreyrnani. Pp. 477-80 in: 'Biology of Australian Frogs and Reptiles'. Eds G. Grigg, R. Shine & H. Ehmann. (Surrey Beatty & Sons: Sydney.) Sadlier, R. A. 1986. A review of the scincid lizards of New Caledonia. Records of the Australian Museum 39, 1-66. Shea, G. M. 1987. Oviparity in Leiolopisma jigurru and a brief review of reproductive mode in Leiolopisma. Herpetological Reviews 18, 29-32. Smith, M. A. 1935. 'Fauna of British India. 11. Sauria.' (Taylor & Francis: London.) xiii+440 pp. Smith, M. A. 1937. A review of the genus Lygosoma and its allies. Records of the Indian Museum 39, 213-34. Zug, G. R. 1985. A new skink (Reptilia : Sauria : Leiolopisma) from Fiji. Proceedings of the Biological Society of Washington 98, 221-31.
Appendix I.
Sources of Data
Names of collections holding voucher specimens abbreviated following Leviton et a/. (1985); other collection abbreviations: CD, specimens provided by Dr C. H. Daugherty, Victoria University, Wellington, New Zealand; LTU, La Trobe University; SB, specimens collected by S. Burgin.
Sources of Plasma Samples Used Bassiana duperreyi: AMS R104777, 3 km W. of Collector, N.S.W.; SAMA R32954, R32956-61, 16 km W. of Penola, S.A. Bassianaplatynotum, AMS R120856, Woodford, N.S.W. Caledoniscincus austrocaledonicus, SAMA R33Ol5, R33017- 18, R33020. Niveoscincus coventryi: NMV D60524, Mt St Leonard, Vic.; NMV D62067-88, 6 km NE. of Beech Forest, Vic. Niveoscincus greeni, TMH C545-60, Mt Rufus, Tas. Niveoscincus metallicus: AMS R97866, Pine Lake, Tas.; NMV D60512, Westernport Bay, Vic. Niveoscincus microlepidotus, TMH C625-56, Mt Eliza, Tas. Niveoscincus ocellatus, TMH C412-28, Cynthia Bay, Lake St Clair, Tas. Niveoscincus orocryptus, TMH C658-78, Mt Eliza, Tas. Niveoscincus palfreymani, AMS R122005, Pedra Branca Rock, Tas. Niveoscincus pretiosus, QVML 1987/3/73, Albatross I., Tas. Cyclodina oliveri, CD 1034, New Zealand. Emoia longicauda, AMS R122624-25, R122627, R122630-3 1, R122633, R122638-40, Southern Highland Province, Papua New Guinea. Eugongylus rufescens, AMS R111369-75, Wau, Papua New Guinea. Cautula zia, SB 442, Wiangarie, N.S.W. Lampropholis challengeri, SB 548, Neutral Bay, N.S.W. Lampropholis guichenoti, SB 530, Macquarie University, Sydney, N.S.W. Leiolopisma telfairii, CD 2022, Round Island, Mauritius. 'Leiolopisma' grande, CD 1055-56, Central Otago, New Zealand. 'Leiolopisma' lichenigerum, captive, Balls Pyramid, Lord Howe I. 'Leiolopisma' nigrofasciolatum, AMS R125819-20, Mare I., Loyalty I. Morethia adelaidensis: SAMA R32534, Wingfield, S.A.; R33203-4, R33220-34, R33297-99, St Kilda, S.A. Morethia boulengeri, AMS R96292, Kandos, N.S.W. Morethia lineoocellata, SAMA R22921, Rottnest Island, W.A. Morethia obscura, SAMA R24803, 20 km SE. of Oodlawirra, S.A. Morethia taeniopleura, QM 546080, Yarraman, Qld. 'Nannoscincus' maccoyi NMV D60520, Mt St Leonard, Vic. Pseudemoia entrecasteauxii group 1, QVML 1986/3/6, 5 km E. of Evandale, Tas. Pseudemoia entrecasteauxii group 2: SAMA R181322, Reevesby I., S.A.; NMV D59877, D59904-5, D59907, D59916-18, 5 km E. of Dreeite, Vic. Pseudemoia spenceri, AMS R122952, Jenolan Caves, N.S.W. Bartleia jigurru, QM 540041, Mt Bartle Frere, Qld. Specimens Examined for Osteological Data (i) Eugongylus group
Bassiana duperreyi: LTU 85/57, La Trobe University campus, Vic; LTU 85/58, south Gippsland. Bassiana platynotum, LTU 86/4, N.S.W. Bassiana trilineata: LTU 85/59, East Mt Barron, W.A.; NMV D933, D1205-6, W.A. (X-rays). Carlia amax, NMV D50450-51, Groote Eylandt, N.T. (X-rays). Carlia bicarinata, LTU 85/72, Wangetti Beach, Cairns, Qld. Carlia jarnoldae, NMV D13916, Oakey Ck, 16 km W. of Cooktown, Qld (X-ray). Carlia pectorialis, LTU 85/74, Bluff, Qld. Carlia tetradactyla: LTU 85/70, Eurora, Vic.; LTU 85/71, Lurg, Vic. Carlia triacantha: NMV D10760, 19.3 km E. of Katherine, N.T. (X-ray); NMV D41626-27, Lake Argyle, W.A. (X-rays). Cautula zia, LTU 86/32, Wiangaree State Forest, N.S.W. Cryptoblepharus virgatus, LTU 85/64, Coffin Bay,
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S.A. Cyclodina ornata: NMV D3724, Warkworth, New Zealand; NMV D2951, New Zealand (X-ray). Emoia atrocostata: NMV D54175, Guadalcanal, Solomon Is; NMV D54176-77, D54179, Gaudalcanal, Solomon Is (X-rays). Emoia cyanura, LTU 85/43, Upolu, Western Samoa. Ernoia nigra: NMV D54173, Guadalcanal, Solomon Is; NMV D54170-71, Guadalcanal, Solomon Is (X-rays). Emoia samoensis, LTU 85/42, Upolu, Western Samoa. Eugongylus rufescens: NMV D6644, Murray I., Torres Strait, Qld; NMV D38573, Oriomo Station, Papua New Guinea (X-ray). Lampropholis challengeri, LTU 85/69, Wiangaree State Forest, N.S.W. Lampropholis cf delicata, LTU 85/66, Mt Lewis, Qld. Larnpropholis guichenoti: LTU 85/65, Stradbroke West, Vic.; LTU 85/149, Healesville, Vic. Lampropholis mustelina: LTU 85/67, Stradbroke West, Vic.; LTU 85/68, Packenham Upper, Vic. 'Leiolopisma' n. maccanni: NMV D2967-68, Wanganuie (sic), New Zealand (X-rays); NMV D3710-11, D3717, New Zealand (X-rays). 'Leiolopisrna' nigrofasciolatum, AMS R93712, New Caledonia. Leiolopisma telfairii, NMV D3859, Mauritius (X-ray). Lygisaurus foliorum, LTU 85/75, Bluff, Qld. Menetia greyii, LTU 85/76, Emu Bay, Kangaroo I., S.A. Morethia boulengeri, LTU 85/63, Kooloonong, Vic. Morethia obscura, LTU 85/62, Cowell, S.A. Nannoscincus maccoyi, LTU 85/60, Packenham Upper, Vic. Niveoscincus coventryi, LTU 85/2, Vic. Niveoscincus greeni: TMH C556, Mt Rufus, summit, Tas.; LTU 86/11, Mt Barrow, summit, Tas. Niveoscincus metallicus: LTU 85/52, Bayles, Vic.; LTU 86/13, Bronte Park, Tas. Niveoscincus microlepidotus, LTU 86/2, 86/17, 86/19, Mt Wellington summit, Tas. Niveoscincus ocellatus: LTU 85/55, Hamilton, Tas; LTU 86/3, Bicheno, Tas. Niveoscincus orocryptus, TMH C662-663, Mt Eliza, Tas. Niveoscincuspretiosus: LTU 86/16, Mt Wellington, Tas.; LTU 86/18, Legana, Tas. Pseudemoia baudini LTU 86/28, Wanna, S.A. Pseudemoia entrecasteauxii gp 1: LTU 85/54, La Trobe University campus, Vic.; LTU 86/23, Avalon, Vic.; LTU 86/31, Mt Wills, Vic. Pseudemoia entrecasteauxii gp 2: LTU 85/48, Woodside East, Vic.; LTU 85/49, Mt St Leonard, Vic.; LTU 85/50-51, Dreeite, Vic.; LTU 86/25, Mt Baw Baw, Vic.; LTU 86/26, Mt Disappointment, Vic. Pseudemoia rawlinsoni: LTU 85/46, Woodside East, Vic.; LTU 85/47, Bayles, Vic. Pseudemoia spenceri: LTU 85/53-54, Vic.; LTU 86/15, Mt Sabine, Otway Ranges, Vic.; LTU 86/30, Mt Baw Baw, Vic. (ii) Sphenomorphus group Ctenotus alacer, LTU 85/77, Flynn's Grave, Alice Springs, N.T. Ctenotus brachyonyx, LTU 85/78, Rockhole Bore, Sunset Country, Vic. Ctenotus brooksi, LTU 85/79, 20 km S. of Alawoona, S.A. Ctenotus essingtonii, LTU 85/80, Djawamba Massif, Eastern Arnhem Land, N.T. Ctenotus regius, LTU 85/81, Whyalla, S.A. Ctenotus robustus: LTU 85/82, Harrow, Vic.; LTU 85/83, Bulla, Vic. Ctenotus taeniolatus, LTU 85/85, Pilot Range, Vic. Eremiascincus richardsonii: LTU 85/102, 35 km NNE. of Bourke, N.S.W.; NMV D457, Illamurta, James Range, N.T. (X-ray); NMV D2936, Tennant Creek, N.T. (X-ray). Eulamprus murrayi, LTU 85/104, Maleny, Qld. Eularnprus gyoyii, LTU 85/106, no data. Eulamprus tympanum, LTU 85/107, Mt Baw Baw, Vic. Gnypetoscincus gueenslandiae, LTU 85/111, Atherton Tableland, Qld. Sphenomorphus concinnatus, NMV D54180, Guadalcanal, Solomon Is. Sphenomorphus sanctus, LTU 86/24, Carita, Java. (iii) Egernia group Egernia coventryi, LTU 85/15, Boneo, Vic. Egernia cunninghami, LTU 85/13, Mt Wombat, Strathbogie Ranges, Vic. Egernia inornata, LTU 85/17, Hattah, Vic. Egernia major, LTU 85/12, Mt Nebo, Qld. Egernia saxatilis, LTU 85/16, Genoa Peak, Vic. Egernia stokesii, LTU 85/14, Uno Hill, S.A. Egernia whitii: 85/18, Too Rour, Strathbogie Ranges, Vic.; LTU 85/21, Banyule Flats, Vic. (iv) Other lygosomines Lamprolepis smaragdina: NMV D54167, Shortland I., Solomon Is; NMV D54168, Shortland I., Solomon Is (X-ray). Lygosoma fernandi, LTU 85/26-27, Kivu, Zaire. Mabuya maculilabris, LTU 85/24-25, Kinshasa, Zaire. Mabuya multifasciata, LTU 85/1, 85/4, Rakata, Krakatau Group, Indonesia. Mabuya striata, LTU 85/28, Pretoria, South Africa. Tribolonotus schmidti: NMV D54192-93, Guadalcanal, Solomon Is; NMV D45194-95, Guadalcanal, Solomon Is (X-rays). (v) Other skinks Chalcides ocellatus, LTU 85/38, Europe (no data). Eumeces fasciatus, LTU 85/33-34, New Albany, Indiana, U.S.A. Eumeces inexpectatus, LTU 85/35, Cedar Key, Florida, U.S.A. Eumeces obsoletus, NMV D9916, D9918, 1 . 6 km W., 8 km N. of Lawrence, Kansas, U.S.A. (X-rays). Gongylomorphus bojeri, NMV D3882, Mauritius.
Generic Revision of Leiolopisma
Appendix 11. Polarity of Morphological Character States Frontoparietal shields. The paired state is by far the more common state in all normally proportioned skinks and is regarded here as plesiomorphic. Fused frontoparietals have evidently been acquired independently many times; in some such taxa the interparietal retains a size close to half that of the frontoparietal region, but in others it may show an apomorphic reduction in size or fusion with the frontoparietal. Rostral-frontonasal suture. This structure, which reflects the separation of the nasal scales, is variable to the extent that it is difficult to determine the plesiomorphic state in skinks. However, in outgroup genera such as pentadactyle scincines, and many other lygosomines, the nasals (or supranasals if present) are closely apposed, if not touching, so that broad separation, as occurs in Cautula, is very probably apomorphic. Size and shape of the palpebral disc. All Australian members of the Eugongylus group have a palpebral disc, so that at this level the presence of this lower eyelid character state is plesiomorphic. In those genera possessing the disc, it appears likely that larger size is apomorphic with respect to smaller. In the species under study, the enlarged and subcircular disc seen in P. spenceri and the L. baudini complex is unique, and regarded here as apomorphic. Palatal bone configuration. The medial margins of the palatal rami of the pterygoids are smooth and unexpanded in most skinks, as in most lizards, and this is no doubt the plesiomorphic state (Greer 1974). The development of pterygoid processes (the beta palate of Greer & Parker 1968) is therefore apomorphic. Shape of contact between nasal and premaxilla. The nasal processes of the premaxillae in skinks typically form a narrowly tapering, V-shaped wedge separating the anterior parts of the nasals. A distinctive and probably apomorphic modification seen in some genera is for the nasal processes to be markedly laterally expanded, so that contact with the nasals is also broadened to form a W-shaped line. A further result of this broadening is increased separation of the external nares, possibly reflected externally in the increased separation of the nasal scales discussed above. Upper temporal fenestra. Possession of an open upper temporal fenestra is a plesiomorphic character state in skinks, although the family shows a tendency to reduce the opening via posterior expansion of the postfrontal (Estes et al. 1988). In many skinks the opening, although reduced compared with some lizard families, persists as an elongate, elliptical slot. In several skink taxa however, the postfrontal completely seals the fenestra, and this is regarded here as apomorphic. This polarity is reinforced by ontogenetic data (Hikida 1978) showing progressive closure of the upper temporal fenestra in Eumeces. Presacral vertebrae. Hoffstetter and Gasc (1969) show that 26 is the probable plesiomorphic presacral count in skinks and other lizards. Pengilley (1972) presented data showing that the Eugongylus group is characterised by an elevated count, usually to 27 or 28. This count is regarded here as plesiomorphic for the Eugongylus group, with still higher counts (ranging 30 or more) treated as apomorphic. Mode of reproduction.
Viviparity is a derived reproductive mode compared with oviparity.
Presence of sex chromosomes. Most skinks, like most lizards, lack sex chromosome heteromorphism. In the Eugongylus group most taxa examined by Donnellan (1985) lacked such heteromorphism, but several genera were composed entirely of species showing a pair seven X Y system. Such taxa are regarded here as sharing an apomorphic character state. Bright ventral pigmentation. This character state appears sporadically throughout the Scincidae, and is difficult to survey due to the loss of, especially, yellow pigments in alcohol-preserved specimens. However, the presence of such colouring is generally the exception rather than the rule in particular lineages, and its absence is here regarded as plesiomorphic and its presence apomorphic. Sexual dichromatism. Within lygosomines, sexual dichromatism is present in some taxa but absent in most, implying multiple derivations or losses. Within the Egernia group, Sphenomorphus group and Eugongylus group it is generally absent, so that its presence in one or two lineages is regarded here as apomorphic. Proportions of head, body and limbs. Skinks of the Eugongylus group, like most skinks, have relatively deep heads and bodies that are squarish in cross-section, and although skinks are well known for limb degeneration, most actually have well developed limbs which contact or overlap when
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adpressed. These proportions are considered here as plesiomorphic. Two opposing trends, towards scansoriality or fossoriality, have led to two apomorphic sets of proportions. Most scansorial species have developed a pronounced dorso-ventral flattening, presumably associated with crevice-dwelling habits, and the limbs and toes are usually especially long. Fossorial or grass-swimming species show reduction in relative limb length, so that limbs generally fail to contact when adpressed.
Manuscript received 31 October 1989; accepted 6 March 1990
