A mitochondrial phylogeny of the rainforest skink genus Saproscincus, Wells and Wellington (1984)

Abstract

The phylogenetic relationships and historical biogeography of 10 currently described rainforest skinks in the genus Saproscincus were investigated using mitochondrial protein-coding ND4 and ribosomal RNA 16S genes. A robust phylogeny is inferred using both maximum likelihood and Bayesian analysis, with all inter-specific nodes strongly supported when datasets are combined. The phylogeny supports the recognition of two major lineages (northern and southern), each of which comprises two divergent clades. Both northern and southern lineages have comparably divergent representatives in mid-east Queensland (MEQ), providing further molecular evidence for the importance of two major biogeographic breaks, the St. Lawrence gap and Burdekin gap separating MEQ from southern and northern counterparts respectively. Vicariance associated with the fragmentation and contraction of temperate rainforest during the mid-late Miocene epoch underpins the deep divergence between morphologically conservative lineages in at least three instances. In contrast, one species, Saproscincus oriarus, shows very low sequence divergence but distinct morphological and ecological differentiation from its allopatric sister clade within Saproscincus mustelinus. These results suggest that while vicariance has played a prominent role in diversification and historical biogeography of Saproscincus, divergent selection may also be important.

Introduction

Pronounced historical changes in the distribution of eastern Australian rainforests have greatly shaped current patterns of diversity of rainforest-restricted fauna. Since the mid-Miocene Australian temperate rainforest has undergone extensive contraction and fragmentation, resulting in what is today a ‘mesothermal archipelago’ of closed forest isolates restricted to the eastern margin (Galloway and Kemp, 1981, Macphail, 1997, Nix, 1982). This has provided a model system for studies of historical biogeography, particularly regarding the role of historic isolation in speciation processes (Hugall et al., 2003, James and Moritz, 2000, Joseph and Moritz, 1993, Moritz et al., 1997, Stuart-Fox et al., 2001). These studies have shown consistent patterns of vicariance across biogeographic barriers that have shaped phylogenetic diversity within a broad range of taxa. However, most studies to date have focused on specific sub-regions of eastern Australia, most notably the Wet Tropics (WT) of Northern Queensland (reviewed in Moritz et al., 2000), while relatively few studies have investigated biogeographic and phylogenetic affinities of rainforest-restricted taxa across the entire mesothermal archipelago (but see Hoskin et al., 2003, Hugall et al., 2003, O’Connor and Moritz, 2003).

At the broader scale, two important biogeographic barriers have been identified: the Burdekin Gap separating the WT from mid-eastern Queensland (MEQ) and the St. Lawrence Gap separating MEQ from south-eastern Queensland (SEQ) and north-eastern New South Wales (NENSW) (Fig. 1). In a preliminary phylogeographic study of three rainforest associated birds, Joseph and Moritz (1993) identified greater affinity of MEQ populations with those of SEQ for the two most rainforest restricted species; the Large-billed Scrubwren (Sericornis magnirostris) and Eastern Whipbird (Psophodes olivaceus). Similarly, in a study integrating palaeo-distributional modeling with a molecular phylogeny of camaenid snails, Hugall et al. (2003) showed that the earliest separations were between WT and MEQ, followed by MEQ and species found in SEQ; moreover, palaeo-distribution models representing cooler and wetter climates predicted substantial connectivity between MEQ and SEQ while the Burdekin gap persisted in isolating NQ. Although these studies suggest that the Burdekin Gap potentially represented a greater biogeographic barrier than the St. Lawrence Gap, other recent published phylogenies have yielded a more complex history with certain clades further supporting the greater connection between MEQ and SEQ, while others indicate a more recent connection between NQ and MEQ (Hoskin et al., 2003, O’Connor and Moritz, 2003). Additional studies examining biogeographic affinities among taxa spanning eastern Australia are therefore required to identify patterns of concordance.

The rainforest skinks of the genus Saproscincus represent an ideal group with which to examine the historical biogeography of eastern Australian rainforests. The genus includes 10 currently described species distributed from the WT to the temperate mesic forests of south-eastern Australia. All members of Saproscincus, with the exception of the most southern species (Saproscincus mustelinus), are rainforest obligates with an overall preference for warm to temperate rainforest formations. Moreover, the group is not found in dry rainforest formations (vine thicket, see Fig. 1), suggesting that annual mean rainfall greater that 1000 mm is an important determinant of species distributions. Given the restriction of Saproscincus to mesic rainforest and the long history of fragmentation of this forest type, biogeographic processes are likely to have been instrumental in diversification of this genus.

Based on previous, primarily morphological evidence, Greer and Kluge (1980) recognised two major groups within the genus; a northern lineage comprising five species (S. basiliscus, S. lewisi, S. czechurai, S. tetradactyla, and S. hannahae) and a southern assemblage also represented by five species (S. challengeri, S. rosei, S. spectabilis, S. mustelinus, and S. oriarus) (Couper and Keim, 1998, Greer and Kluge, 1980, Sadlier et al., 1993). Using phylogenetic analysis of a limited number of morphological traits, Greer (1989) concluded that the northern lineage is defined by five derived states: smaller size (maximum SVL = 47 mm), a unique arrangement of the nuchal scales; an elevated number of premaxillary teeth (13 or more); and by having a constant clutch size of two (Greer, 1989). While this separation is well supported morphologically, biogeographic delineation is less clear. The two groups are allopatrically distributed except for overlap in MEQ. Members of the Northern lineage are restricted primarily to the WT with the single exception of S. hannahae, an endemic of MEQ (Couper and Keim, 1998). Members of the southern group, which was not defined by any derived states and may not be monophyletic, are distributed from the subtropics to the cool temperate regions of eastern Australia. The exception to this, however, is an undescribed species that, although having strong morphological affinities to the southern group, is restricted to high elevations in MEQ (P. Couper, Queensland Museum, personal communication).

Until recently, 6 of the 10 currently recognised species constituted two complexes (Couper and Keim, 1998, Sadlier, 1998) and there has been no phylogenetic assessment of the genus as a whole. Thus the phylogenetic relationships among members within major groups, particularly the northern one, remain poorly understood. Sadlier et al. (1993) assessed allozymic and morphological variation among members of the southern group identifying S. spectabilis and S. rosei as sister species, but did not include S. mustelinus in the study. Consideration of S. mustelinus is of particular interest as there remains uncertainty regarding whether this species represents a third, yet to be deciphered, complex (Sadlier, 1998, Wells and Wellington, 1985).

Here, we present a molecular phylogeny based on partial sequences of the mitochondrial protein-coding ND4 and ribosomal RNA 16S genes in order to elucidate the phylogenetic relationships and biogeographic affinities of all members within the genus Saproscincus. In doing so, we also aim to resolve two issues of particular taxonomic interest: (1) the phylogenetic placement of the undescribed species from MEQ, that is, whether there is molecular confirmation of its affinity with the southern group; and (2) whether there exists genetic divergence within the mustelinus complex, comparable to interspecific divergence within the genus. Answers to these questions will contribute to our growing knowledge of speciation processes and historical biogeography of this rainforest fauna (Moritz et al., 2000).