Abstract

We examined the comparative phylogeography of all species within the endemic New Zealand skink genus Cyclodina to gain insight into the influence of historical processes on the biogeography of the North Island fauna. Until 1–2 kya, six Cyclodina species occurred sympatrically across the North Island of New Zealand. However, most species have undergone dramatic distributional declines subsequent to the introduction of mammals and the arrival of humans. We compare the phylogeographic patterns evident in Cyclodina species in three biogeographic categories: widespread species (Cyclodina aenea, Cyclodina ornata), North Island disjunct relics (Cyclodina macgregori, Cyclodina whitakeri), and northeastern island relics (Cyclodina alani, Cyclodina oliveri, Cyclodina townsi). Mitochondrial DNA (ND2) sequence data was obtained from across the entire range of each Cyclodina species. We used Neighbour-joining, maximum likelihood and Bayesian methods to examine the phylogeographic patterns present in each species. Phylogeographic patterns varied among species in different biogeographic categories. Substantial phylogeographic structure was evident in the two widespread species (C. aenea, C. ornata), with Pliocene and Pleistocene divergences between clades evident. Divergences among island groups in the three northeastern island relic species (C. alani, C. oliveri, C. townsi) occurred during the late Pliocene–Pleistocene. By contrast, relatively shallow structure, indicative of late Pleistocene divergences, was present in the two North Island disjunct species (C. macgregori, C. whitakeri). The results strongly suggest that the Poor Knights Islands population of C. ornata represents a new species. We suggest that the contrasting phylogeographic patterns exhibited by Cyclodina species in different biogeographic categories might be related to body size, ecology, and habitat preferences.

INTRODUCTION

The New Zealand archipelago has experienced a complex climatic and geological history subsequent to the Pliocene (Cooper & Millener, 1993; Markgraf, McGlone & Hope, 1995; Worthy & Holdaway, 2002). However, the historical processes that have shaped the North Island of New Zealand differed markedly to the processes that have been responsible for shaping the landscape of the South Island (Fig. 1). The Southern Alps that characterize the South Island were formed by tectonic activity along the alpine fault line, which commenced during the Miocene, and intensified during the Pliocene and early Pleistocene (Gage, 1980; King, 2000). The presence of mountainous regions in the South Island has facilitated extensive glaciation since the late Pliocene, created an expansive alpine zone, and fundamentally altered climatic conditions and prevailing weather patterns (Suggate, 1990; Pillans, 1991; Worthy & Holdaway, 2002). However, the North Island largely escaped the combined impacts of rapid tectonic uplift and glaciation (Suggate, 1990; Pillans, 1991). Instead, volcanic activity and repeated fluctuations in sea level associated with Pleistocene glacial cycles have been the predominant forces that have shaped the North Island landscape. Pleistocene glacial cycles resulted in sea level fluctuations leading to the continual connection and separation of offshore islands to the adjacent mainland (Fleming, 1979; Suggate, 1990). Volcanism has played a dominant role in modifying the landscape of the North Island subsequent to the late Pliocene (McDowall, 1996; Worthy & Holdaway, 2002). For example, the Central Plateau region has experienced substantial volcanic eruptions centred around Lake Taupo (a volcanic lake), which has erupted approximately 28 times over the last 250 kyr (McDowall, 1996; Worthy & Holdaway, 2002).

Figure 1.

Major geographic regions in New Zealand.

Figure 1.

Major geographic regions in New Zealand.

Although several molecular studies have examined the impact of historical processes, such as Pliocene mountain building, on the biogeographic patterns of the South Island fauna (Buckley, Simon & Chambers, 2001; Trewick, 2001; Chinn & Gemmell, 2004; Trewick & Morgan-Richards, 2005), less attention has been paid to the biogeographic patterns evident in the North Island fauna. In the North Island, two major biogeographic patterns appear to be evident: (1) high levels of species diversity and endemism in the northern half of the island (Northland; Fig. 1) and (2) the presence of a biogeographic barrier in the Central Plateau region. Pleistocene sea level fluctuations are believed to have influenced the evolution of the North Island biota, particularly in the Northland region, which existed as an archipelago of low-lying islands during periods of elevated sea level (Fleming, 1979; Hayward, 1986). The repeated connection and separation of islands in the Northland region during the Pleistocene appears to have resulted in substantial levels of population structuring and speciation in both plant (Gardner et al., 2004) and animal taxa (Morgan-Richards, 1997; Gleeson, Howitt & Ling, 1999; Lloyd, 2003a, b; Morgan-Richards & Wallis, 2003; Berry & Gleeson, 2005; Spencer, Brook & Kennedy, 2006; Hare, Daugherty & Chapple, 2008).

Geological evidence suggests that eruptions from Central Plateau volcanoes over the past 2 Myr resulted in the repeated destruction of forests and vegetation across vast regions of the central North Island (McDowall, 1996; Worthy & Holdaway, 2002). Such eruptions would have potentially created gaps in the distribution of plant and animal taxa across the central North Island (McDowall, 1996), genetically isolating populations on each side of the Central Plateau until revegetation enabled recolonization of the region (Lloyd, 2003a, b). However, other explanations apart from volcanic activity have been suggested for the Central Plateau region (approximately 38–39°S; also called the Taupo line) representing a significant biogeographic barrier for plant (Wardle, 1963; Connor, 2002) and vertebrate taxa (McCann, 1955; Bull & Whitaker, 1975; Towns, Daugherty & Newman, 1985). The depauperate flora of the lower North Island may be the result of the combined effects of Pliocene marine inundation and tectonic activity (Rogers, 1989; Worthy & Holdaway, 2002). However, because the Northland region was dominated by expansive Kauri forests (until the arrival of humans), which were not widespread in the lower North Island (Worthy & Holdaway, 2002), ecological factors might also explain the presence of the Central Plateau biogeographic barrier.

Few studies have investigated the phylogeographic patterns that are evident in species that are widely distributed across the North Island (e.g. weta, Hemideina thoracica White: Morgan-Richards, 1997; Morgan-Richards & Wallis, 2003); short-tailed bats, Mystacina tuberculata Gray: Lloyd, 2003a, b). In the present study, we examine the comparative phylogeography of all species in the endemic New Zealand skink genus Cyclodina to gain insight into the influence of historical processes on the biogeography of the North Island fauna. Cyclodina contains nine described species, including three recently described species (Chapple et al., 2008a,b), whose distributions are restricted to the North Island and outlying islands (Gill & Whitaker, 2001) (Fig. 2, Table 1). Recent molecular studies indicate that Cyclodina is not monophyletic (Hickson, Slack & Lockhart, 2000; Smith et al., 2007; our unpublished data). Towns et al. (1985) summarized the distributional patterns and biogeographic patterns in the New Zealand skink fauna. The copper skink (Cyclodina aenea Girard) and ornate skink (Cyclodina ornata Gray) are both widely distributed across the North Island, with their distribution spanning the Central Plateau region (Fig. 2, Table 1). The distribution of the robust skink (Cyclodina alani Robb) and marbled skink (Cyclodina oliveri McCann) is currently restricted to northeastern offshore Islands, but subfossil evidence (Worthy, 1987, 1991) indicates that until recently (approximately 1–2 kya) they were distributed continuously across the North Island mainland (‘northeastern island relics’; Towns et al., 1985) (Fig. 2, Table 1). Whitaker's skink (Cyclodina whitakeri Hardy) and McGregor's skink (Cyclodina macgregori Robb) both have a disjunct distribution with northeastern island populations and populations in the lower North Island in the Wellington region (Fig. 2), although subfossil evidence (Worthy, 1987, 1991) indicates that both were continually distributed across the south island until recently (‘North Island disjunct relics’, Towns et al., 1985) (Table 1).

Figure 2.

Distribution maps and location of tissue samples used in this study. (A) Cyclodina aenea (circles), Cyclodina aenea‘Te Paki’ (CAE9, CAE20), and Cyclodina aenea‘Poor Knights’ (triangles in the inset for the Poor Knights Islands); (B) Cyclodina ornata; (C) Cyclodina alani (black circles), Cyclodina macgregori (squares) and Cyclodina whitakeri (grey circles); and (D) Cyclodina oliveri (circles) and Cyclodina townsi (squares). Distributional data were obtained from the New Zealand Department of Conservation's BioWeb Herpetofauna Database (2006).

Figure 2.

Distribution maps and location of tissue samples used in this study. (A) Cyclodina aenea (circles), Cyclodina aenea‘Te Paki’ (CAE9, CAE20), and Cyclodina aenea‘Poor Knights’ (triangles in the inset for the Poor Knights Islands); (B) Cyclodina ornata; (C) Cyclodina alani (black circles), Cyclodina macgregori (squares) and Cyclodina whitakeri (grey circles); and (D) Cyclodina oliveri (circles) and Cyclodina townsi (squares). Distributional data were obtained from the New Zealand Department of Conservation's BioWeb Herpetofauna Database (2006).

Table 1.

Summary of the habitat preferences, body size, present distribution and past distribution of Cyclodina species

Species Habitat Body size (mm SVL) Present distribution Past distribution 
Cyclodina aenea Forested habitats, preferring open or shaded habitats with ground cover1 621,2 Widespread throughout NI from Northland to Wellington1,3 Widespread throughout NI from Northland to Wellington1,3 
Cyclodina aenea‘Poor Knights’ Flax and scrub habitats with ground cover4 624 Poor Knights Islands5 Poor Knights Islands5 
Cyclodina aenea‘Te Paki’ Unknown5 ?5 Northern tip of Northland5 Unknown5 
Cyclodina alani Low coastal forest1 1421 Matapia I, Moturoa I, Mokohinau Islands (Tatapihi [Groper] I), Mercury Islands (Middle I, Green I), Castle I. Translocated to Mercury Islands (Korapuki I, Stanley I, Red Mercury I) & Motuopao I3,6 Lowland coastal forest from Northland to the Wellington region, & offshore islands around the northwest, northeast & southwest3,7–9 
Cyclodina macgregori Leaf litter under coastal forest and scrub1 1121,2 Cavalli Islands (Motuharakeke I), Outer Bream Islands (Muitaha I), Hen & Chickens Group (Sail Rock), Mana I near Wellington. Translocated to Hen & Chickens Group (Lady Alice I)3,6 NI from Northland to Wellington & many offshore islands3,7,8 
Cyclodina oliveri Leaf litter under coastal forest and scrub1 1161,4 Poor Knights Islands, Ohinau Islands (Old Man Rock), Mercury Islands (Middle I, Green I), Alderman Islands Translocated to Mercury Islands (Korapuki I)1,3,6 Northland to the northern Bay of Plenty6–8
Cyclodina townsi Broadleaf forest and low scrub10 8710 Mokohinau Islands (Tatapihi [Groper] I, Stack ‘H’), Hen & Chickens Group (Muriwhenua I, Wareware I, Pupuha I, One I, Middle stack), Little Barrier I, Great Barrier I. Translocated to Hen & Chickens Group (Lady Alice I, Whatupuke I, Coppermine I)10 Northland to the northern Bay of Plenty6–8
Cyclodina ornata Forest or open areas with stable cover1 801,2 Widespread through NI from the Three Kings Islands to Wellington1,3 Widespread through NI from the Three Kings Islands to Wellington1,3 
Cyclodina whitakeri Coastal forest and scrub1 1011 Mercury Islands (Middle I), Castle I, Pukerua Bay north of Wellington. Translocated to Mercury Islands (Korapuki I, Stanley I, Red Mercury I)1,3,6 lowland forest through the NI from Northland to the Wellington region & islands of the Hauraki Gulf6–8 
Species Habitat Body size (mm SVL) Present distribution Past distribution 
Cyclodina aenea Forested habitats, preferring open or shaded habitats with ground cover1 621,2 Widespread throughout NI from Northland to Wellington1,3 Widespread throughout NI from Northland to Wellington1,3 
Cyclodina aenea‘Poor Knights’ Flax and scrub habitats with ground cover4 624 Poor Knights Islands5 Poor Knights Islands5 
Cyclodina aenea‘Te Paki’ Unknown5 ?5 Northern tip of Northland5 Unknown5 
Cyclodina alani Low coastal forest1 1421 Matapia I, Moturoa I, Mokohinau Islands (Tatapihi [Groper] I), Mercury Islands (Middle I, Green I), Castle I. Translocated to Mercury Islands (Korapuki I, Stanley I, Red Mercury I) & Motuopao I3,6 Lowland coastal forest from Northland to the Wellington region, & offshore islands around the northwest, northeast & southwest3,7–9 
Cyclodina macgregori Leaf litter under coastal forest and scrub1 1121,2 Cavalli Islands (Motuharakeke I), Outer Bream Islands (Muitaha I), Hen & Chickens Group (Sail Rock), Mana I near Wellington. Translocated to Hen & Chickens Group (Lady Alice I)3,6 NI from Northland to Wellington & many offshore islands3,7,8 
Cyclodina oliveri Leaf litter under coastal forest and scrub1 1161,4 Poor Knights Islands, Ohinau Islands (Old Man Rock), Mercury Islands (Middle I, Green I), Alderman Islands Translocated to Mercury Islands (Korapuki I)1,3,6 Northland to the northern Bay of Plenty6–8
Cyclodina townsi Broadleaf forest and low scrub10 8710 Mokohinau Islands (Tatapihi [Groper] I, Stack ‘H’), Hen & Chickens Group (Muriwhenua I, Wareware I, Pupuha I, One I, Middle stack), Little Barrier I, Great Barrier I. Translocated to Hen & Chickens Group (Lady Alice I, Whatupuke I, Coppermine I)10 Northland to the northern Bay of Plenty6–8
Cyclodina ornata Forest or open areas with stable cover1 801,2 Widespread through NI from the Three Kings Islands to Wellington1,3 Widespread through NI from the Three Kings Islands to Wellington1,3 
Cyclodina whitakeri Coastal forest and scrub1 1011 Mercury Islands (Middle I), Castle I, Pukerua Bay north of Wellington. Translocated to Mercury Islands (Korapuki I, Stanley I, Red Mercury I)1,3,6 lowland forest through the NI from Northland to the Wellington region & islands of the Hauraki Gulf6–8 

For more detailed information on the current distribution of Cyclodina species, see Fig. 2. Body size refers to maximum body size. NI, North Island; SVL, snout–vent length.

*

It is unknown whether these subfossils relate to C. oliveri or C. townsi (D. G. Chapple, G. B. Patterson, D. M. Gleeson, C. H. Daugherty & P. A. Ritchie, unpubl. data).

We examine the comparative phylogeography of Cyclodina species using mitochondrial (mt)DNA sequence data (ND2) from across the entire distribution of each species. It has been hypothesized that the low levels of genetic variation evident across the range of Cyclodina species with relictual distributions (e.g. C. macgregori, C. whitakeri) are due to the extinction of intervening populations of a previously continuously distributed species, rather than the loss of genetic variation in association with recent population declines (Towns & Daugherty, 1994; Towns, Daugherty & Cree, 2001). Because six Cyclodina species were widely distributed across the North Island 1–2 kya (Worthy, 1987, 1991; Towns & Daugherty, 1994; Towns et al., 2001; BioWeb Herpetofauna Database, 2006; Table 1), each species should still possess the genetic imprint of this former distribution. We also complete topology tests to examine several taxonomic issues within Cyclodina.

Background to the skink genusCyclodina

There are seven described Cyclodina species: six extant (Gill & Whitaker, 2001) and one extinct (C. northlandi Worthy, Worthy, 1991). Recent taxonomic work has resulted in the description of three new Cyclodina species: C. townsi (Chapple et al., 2008a), C. aenea‘Poor Knights Islands’ and C. aenea‘Te Paki’ (Chapple et al., 2008b), increasing the number of described species to 10’. Hardy (1977) also suggested that the Poor Knights Islands and Three Kings Islands populations of C. ornata were morphologically distinctive, and possibly represent distinct species. Recent molecular studies have suggested that Cyclodina is not monophyletic (Hickson et al., 2000; Smith et al., 2007; our unpublished data).

Morphological and ecological differences distinguish Cyclodina from Oligosoma, the other endemic skink genus in New Zealand (Patterson & Daugherty, 1995). Cyclodina are crepuscular to nocturnal species that inhabit shaded and forested habitats (Table 1), whereas Oligosoma contains diurnal species that inhabit more open habitats (Patterson & Daugherty, 1995; Gill & Whitaker, 2001). Oligosoma is more diverse than Cyclodina, with 24 described species (23 extant, one extinct species; Gill & Whitaker, 2001; Chapple & Patterson, 2007). Although Oligosoma species generally have widespread distributions across the North Island, South Island, and Stewart Island, no species is continuously distributed across the North Island (Gill & Whitaker, 2001).

MATERIAL AND METHODS

Taxonomic sampling

We obtained samples from all described species in the New Zealand skink genus Cyclodina (Fig. 2; see also Supporting Information, Table S1). Samples were obtained primarily from the National Frozen Tissue Collection (Victoria University of Wellington, New Zealand) and ethanol preserved specimens housed at Te Papa (National Museum of New Zealand, Wellington). Our sampling encompassed populations from across the entire distribution of each Cyclodina species: C. alani (seven samples), C. aenea (38 samples), C. aenea‘Poor Knights’ (five samples), C. aenea‘Te Paki’ (two samples), C. macgregori (four samples), C. oliveri McCann (three samples), C. townsi (three samples), C. ornata (24 samples) and C. whitakeri (seven samples) (Table S1). Because we examine the taxonomy and phylogeography of the C. oliveri species complex in detail elsewhere (Chapple et al., 2008a), we have only included representative samples of C. oliveri and C. oliveri‘Mokohinau’ in the present study. Based on the results of a broader phylogenetic study of the relationships among all members of the New Zealand skink radiation (D. G. Chapple, C. H. Daugherty & P. A. Ritchie, unpubl. data), we included samples from the New Zealand common skink (Oligosoma nigriplantare polychroma Patterson & Daugherty), the speckled skink (Oligosoma infrapunctatum Boulenger), and the Lord Howe Island skink (‘Oligosoma’ lichenigera O'Shaughnessy; sample from South Australian Museum) (Table S1).

DNA extraction, amplification and sequencing

Total genomic DNA was extracted from liver, toe, or tail samples using a modified phenol-chloroform extraction protocol (Sambrook, Fritsch & Maniatis, 1989). For each sample, we targeted a portion of the mitochondrial gene ND2 (approximately 600 bp). This region was chosen because work at comparable taxonomic levels in other squamate reptile groups has indicated useful levels of variability (Greaves et al., 2007, 2008; Hare et al., 2008).

The primers used to amplify and sequence ND2 were L4437 (Macey et al., 1997) and ND2r102 (Sadlier et al., 2004). However, two internal primers were also used to amplify ND2 for some samples (ND2F-infrapunctatum, 5′-GCATGATTYACCGGAAY ATGAGACAT-3′; ND2R-infrapunctatum, 5′-GGGGC AAGKCCTAGTTTTATGG-3′; Greaves et al. (2007). Polymerase chain reaction and sequencing were conducted as described in Greaves et al. (2007).

Sequence data were edited using CONTIGEXPRESS, version 9.1.0 (Invitrogen), and aligned using the default parameters of CLUSTAL X (Thompson et al., 1997). The aligned sequences were translated into amino acid sequences using the vertebrate mitochondrial code to check whether the sequences were truly mitochondrial in origin. Because no premature stop codons were observed, we conclude that all sequences obtained are true mitochondrial copies. Sequence data as submitted to GenBank under accession numbers EF033052, EF033050, EF043106, EF-81173, EF081175–EF081177, EF081182–EF081184, EF081187, EF103954, and EF567120–EF567203.

Phylogenetic analyses

Because Cyclodina is not monophyletic (our unpublished data; see also Hickson et al., 2000; Smith et al., 2007), we split our dataset into two for all phylogenetic analyses: (1) Cyclodina aenea species complex (C. aenea, C. aenea‘Te Paki’, C. aenea‘Poor Knights’) and (2) other Cyclodina (C. alani, C. macgregori, C. oliveri, C. townsi, C. ornata, C. whitakeri).

Neighbour-joining (NJ) analyses, using the Tamura–Nei correction, were conducted in PAUP* v4.0b10 (Swofford, 2002). MODELTEST 3.7 (Posada & Crandall, 1998) was used to determine the most appropriate model of evolution for our dataset, generating log-likelihood scores for the dataset in PAUP* and conducting a hierarchical likelihood ratio test (hRLT). Base frequencies, substitution rates, the proportion of invariant sites (I), and the among-site substitution rate variation were estimated in MODELTEST, with these values implemented in PAUP* to generate a maximum likelihood (ML) tree.

Bayesian analyses were completed using the computer program MrBayes 3.1.2 (Huelsenbeck & Ronquist, 2001). We used the default value of four Markov chains per run, and ran the analysis for one million generations. The chain was sampled every 100 generations to obtain 10 000 sampled trees. The first 2500 sampled trees were discarded as the burn-in phase, with the last 7500 trees used to estimate the Bayesian posterior probabilities. We used both bootstrap values and Bayesian posterior probabilities to assess branch support. NJ bootstraps (1000 replicates) were generated in PAUP*. We consider branches supported by bootstraps values greater than or equal to 70% (Hillis & Bull, 1993), and posterior probability values greater than or equal to 95% (Wilcox et al., 2002) to be significantly supported by our data. Uncorrected genetic distances were calculated in MEGA 3.1 (Kumar, Tamura & Nei, 2004).

Estimating divergence times

To estimate the divergence time of lineages, we calibrated the evolutionary rate of ND2 by re-analysing the data from Macey et al. (1998) for the agamid genus Laudakia. Macey et al. (1998) calibrated this rate through geological dating of tectonic events (mountain uplift) on the Iranian Plateau. The ND2 evolutionary rate has been demonstrated to be consistent (approximately 1.2–1.4%) across several vertebrate groups (fish, amphibians, reptiles; Weisrock et al. (2001). We recalculated the evolutionary rate for Laudakia using only the 550-bp fragment of ND2 used in the present study (Smith et al., 2007). We calculated average between-group nucleotide differences across each of the calibrated nodes from Macey et al. (1998) (1.5, 2.5, and 3.5 Mya), plotted them against time and then used the slope of the linear regression to calculate a rate of evolution for our 550-bp fragment of ND2. This resulted in an evolutionary rate of 1.4% per Myr (0.7% per lineage, per Myr) and is slightly faster than the rate of 1.3% per Myr found by Macey et al. (1998).

Hypothesis testing

We completed Shimodaira–Hasegawa tests in PAUP* (Shimodaira & Hasegawa, 1999; Goldman, Anderson & Rodrigo, 2000) using full optimization and 1000 replicates to examine several alternative topologies in the genus Cyclodina. We tested the significance of the log-likelihood difference between our optimal ML/Bayesian tree (using the ML −ln L) and alternative hypotheses representing three taxonomic hypotheses:

  1. Based on evidence from haem compound electrophoresis, Hardy (1977) considered the Great Barrier Island population of C. aenea to be closely related to the Poor Knights population that has recently been described as a new species (Chapple et al., 2008b). However, the Great Barrier Island population is not morphologically distinctive from the typical C. aenea morphology (Hardy, 1977). We tested the alternative topology that the Great Barrier Island represents a distinct species within the C. aenea species complex;

  2. Hardy (1977) found that the Three Kings Islands population of C. ornata was morphologically distinctive from other C. ornata populations, having higher ventral scale counts. We tested the alternative topology that the Three Kings Islands population of C. ornata represents a distinct species.

  3. Hardy (1977) found that the Poor Knights Islands (Aorangi) population of C. ornata had higher lamella counts compared to other C. ornata populations. We tested the alternative topology that the morphologically distinctive Poor Knights Islands population of C. ornata represents a distinct species.

RESULTS

Cyclodina aeneaspecies complex

The edited alignment comprised 550 characters, of which 179 (33%) were variable and 128 (23%) were parsimony informative. For the ingroup only, the alignment contained 179 (33%) variable characters, of which 51 (9%) were parsimony-informative. Base frequencies were unequal (A = 0.323, T = 0.215, C = 0.333, G = 0.129), but a chi-square test confirmed the homogeneity of base frequencies among sequences (d.f. = 141, P = 0.9705). For one sample (CAE42), only approximately 525 bp of sequence data was obtained, whereas only approximately 325 bp of sequence data was obtained for another sample (CAE41) due to the poor quality of the DNA template.

The hRLT from MODELTEST supported the TrN+G substitution model as the most appropriate for our dataset (−ln L = 2342.5625). Parameters estimated under this model were: relative substitution rates (A ↔ C = 1.0, A ↔ G = 11.32, A ↔ T = 1.0, C ↔ G = 1.0, C ↔ T = 7.64, G ↔ T = 1.00) and gamma shape parameter (0.2758). The topology of the NJ, ML, and Bayesian trees were almost identical, therefore only the optimal ML tree (−ln L = 2427.22515) is shown in Figure 3A, with NJ bootstrap values and Bayesian posterior probabilities indicating branch support. Extremely strong support (100 bootstrap and 0.99–1.0 posterior probability in all cases) exists for the presence of three distinct species within the C. aenea species complex: C. aenea, C. aenea‘Poor Knights Islands’, and C. aenea‘Te Paki’ (Fig. 3A). A substantial level of genetic differentiation is evident between C. aenea and the two new taxa: C. aenea‘Poor Knights Islands’[mean pairwise genetic distance (PGD) = 14.4%] and C. aenea‘Te Paki’ (PGD = 14%). A significant level of genetic divergence is also evident between the two undescribed species (PGD = 11.7%).

Figure 3.

Maximum likelihood (ML) tree for Cyclodina based on 550 bp of the ND2 mitochondrial gene. The topology of the Neighbour-joining (NJ) and Bayesian trees were identical to the ML trees shown. Two measures of branch support are indicated with NJ bootstraps shown on the left and Bayesian posterior probabilities shown on the right (only values over 50 and 0.7, respectively, are shown). Because Cyclodina is not monophyletic, we split our dataset into two for phylogenetic analyses (see text): (A) Cyclodina aenea species complex (nb. clade 2 was recovered in the NJ and Bayesian trees with 69 bootstrap and 0.77 posterior probability, but not the ML tree shown here) and (B) other Cyclodina species.

Figure 3.

Maximum likelihood (ML) tree for Cyclodina based on 550 bp of the ND2 mitochondrial gene. The topology of the Neighbour-joining (NJ) and Bayesian trees were identical to the ML trees shown. Two measures of branch support are indicated with NJ bootstraps shown on the left and Bayesian posterior probabilities shown on the right (only values over 50 and 0.7, respectively, are shown). Because Cyclodina is not monophyletic, we split our dataset into two for phylogenetic analyses (see text): (A) Cyclodina aenea species complex (nb. clade 2 was recovered in the NJ and Bayesian trees with 69 bootstrap and 0.77 posterior probability, but not the ML tree shown here) and (B) other Cyclodina species.

The level of genetic differentiation evident within C. aenea‘Poor Knights Islands’ (restricted to the Poor Knights Islands; PGD = 0.6%; 0.43 Mya) and C. aenea‘Te Paki’ (restricted to northern Northland; PGD = 0.5%; 0.36 Mya) is relatively low, but substantially greater in the more widespread C. aenea (PGD = 2.5%; 1.79 Mya). Five clades are evident within C. aenea, as well as two divergent clades in the Northland region (CAE30: Dargaville, CAE36: Whangarei; Fig. 3A). Clade 1 (99 bootstrap, 1.0 posterior probability; PGD = 0.8%; 0.57 Mya) contains populations from the Alderman Islands, Mercury Islands (Red Mercury Island), Ohinau Island, and the North Island mainland south of the Waikato/Bay of Plenty region (Fig. 4A). Clade 2 (recovered in the NJ and Bayesian trees with 69 bootstrap and 0.77 posterior probability, but not the ML tree shown in Fig. 3A) contains populations from the Mercury Islands (Korapuki Island), the western side of Coromandel Peninsula, and the Auckland region (PGD = 0.6%; 0.43 Mya). Clade 3 (85 bootstrap, 1.0 posterior probability; PGD = 0.4%; 0.29 Mya) comprises populations from Great Barrier Island (Fig. 4A). The Shimodaira–Hasegawa topology test clearly rejected the hypothesis that the Great Barrier Island population represents a distinct species (P < 0.001). Clade 4 (52 bootstrap, 1.0 posterior probability; PGD = 0.6%; 0.43 Mya) contains populations from Little Barrier Island and the Auckland region (Fig. 4A). Clade 5 (96 bootstrap, 1.0 posterior probability) contains populations from the Mokohinau Islands (Fig. 4A). The mean pairwise genetic distances between the five clades and the two divergent Northland samples (CAE30, CAE36) range between 1.2–6.1% (0.86–4.36 Mya) (Table 2).

Figure 4.

Distribution of clades within (A) Cyclodina aenea and (B) Cyclodina ornata identified in Fig. 3.

Figure 4.

Distribution of clades within (A) Cyclodina aenea and (B) Cyclodina ornata identified in Fig. 3.

Table 2.

Uncorrected genetic distance matrix for Cyclodina aenea clades based on 550 bp of the ND2 mitochondrial gene

Clade Clade 1 Clade 2 Clade 3 Clade 4 Clade 5 CAE30 CAE36 
Clade 1 NA       
Clade 2 0.030 NA      
Clade 3 0.036 0.017 NA     
Clade 4 0.042 0.040 0.020 NA    
Clade 5 0.032 0.014 0.013 0.015 NA   
CAE30 0.060 0.052 0.049 0.058 0.047 NA  
CAE36 0.051 0.042 0.041 0.033 0.039 0.061 NA 
Clade Clade 1 Clade 2 Clade 3 Clade 4 Clade 5 CAE30 CAE36 
Clade 1 NA       
Clade 2 0.030 NA      
Clade 3 0.036 0.017 NA     
Clade 4 0.042 0.040 0.020 NA    
Clade 5 0.032 0.014 0.013 0.015 NA   
CAE30 0.060 0.052 0.049 0.058 0.047 NA  
CAE36 0.051 0.042 0.041 0.033 0.039 0.061 NA 

NA, not applicable.

OtherCyclodinaspecies

The edited alignment comprised 550 characters, of which 203 (37%) were variable and 149 (27%) were parsimony informative. For the ingroup only, the alignment contained 203 (37%) variable characters, of which 54 (10%) were parsimony-informative. Base frequencies were unequal (A = 0.327, T = 0.214, C = 0.345, G = 0.114), but a chi-square test confirmed the homogeneity of base frequencies among sequences (d.f. = 150, P = 0.9999). For several samples, only approximately 525 bp of sequence data was obtained (COR13, COR15, COR17, COR25–27). In addition, due to the poor quality of the DNA template, a small number of samples had a reduced sequence length of approximately 325 bp (COR9–10, COR18–19, COR21, COR24).

The hRLT from MODELTEST supported the TrN+G substitution model as the most appropriate for our dataset (−ln L = 3065.2251). Parameters estimated under this model were: relative substitution rates (A ↔ C = 1.0, A ↔ G = 24.81, A ↔ T = 1.0, C ↔ G = 1.0, C ↔ T = 9.65, G ↔ T = 1.00) and gamma shape parameter (0.2464). The topology of the NJ, ML, and Bayesian trees were identical, therefore only the optimal ML tree (−ln L = 3302.01234) is shown in Figure 3B, with NJ bootstrap values and Bayesian posterior probabilities indicating branch support. There is extremely strong support for the monophyly of all described species (C. alani, 93 bootstrap, 1.0 posterior probability; C. macgregori, 100 bootstrap, 1.0 posterior probability; C. oliveri, 100 bootstrap, 1.0 posterior probability; C. ornata, 72 boostrap, 1.0 posterior probability), as well as the recently described Towns' skink (C. townsi, 100 bootstrap, 1.0 posterior probability). The mean pairwise genetic distance between recognized species ranges between 7.5–11.9% (Table 3).

Table 3.

Uncorrected genetic distance matrix for Cyclodina based on 550 bp of the ND2 mitochondrial gene

Species Cyclodina alani Cyclodina macgregori Cyclodina oliveri Cyclodina whitakeri Cyclodina ornata Cyclodina ornata‘PKI’ Cyclodina townsi 
Cyclodina alani NA       
Cyclodina macgregori 0.111 NA      
Cyclodina oliveri 0.103 0.095 NA     
Cyclodina whitakeri 0.092 0.092 0.075 NA    
Cyclodina ornata 0.104 0.111 0.097 0.096 NA   
Cyclodina ornata ‘PKI’ 0.112 0.108 0.104 0.119 0.094 NA  
Cyclodina‘Mokohinau’ 0.112 0.106 0.085 0.086 0.103 0.116 NA 
Species Cyclodina alani Cyclodina macgregori Cyclodina oliveri Cyclodina whitakeri Cyclodina ornata Cyclodina ornata‘PKI’ Cyclodina townsi 
Cyclodina alani NA       
Cyclodina macgregori 0.111 NA      
Cyclodina oliveri 0.103 0.095 NA     
Cyclodina whitakeri 0.092 0.092 0.075 NA    
Cyclodina ornata 0.104 0.111 0.097 0.096 NA   
Cyclodina ornata ‘PKI’ 0.112 0.108 0.104 0.119 0.094 NA  
Cyclodina‘Mokohinau’ 0.112 0.106 0.085 0.086 0.103 0.116 NA 

The Poor Knights Islands population of C. ornata (C. ornata‘PKI’) is considered as a distinct taxa (see text).

NA, not applicable.

Geographic structure is present within C. alani (PGD = 1.8%; 1.29 Mya), with the Matapia Island population (CAL2) clearly divergent from the Castle Island and Mercury Islands populations (PGD Matapia I versus other C. alani = 4.4%; 3.14 Mya) (Fig. 3). Relatively less genetic differentiation was evident between the Castle Island and Mercury Islands populations (PGD = 1.4%; 1 Mya). By contrast, no substantial phylogeographic structure was evident within C. macgregori (PGD = 0.7%; 0.5 Mya), with low levels of genetic divergence between the populations on Mana Island (lower North Island) and Sail Rock in the Hen and Chickens Islands (northeastern North Island) (PGD = 0.7%; 0.5 Mya). Likewise, geographic structuring within C. whitakeri was relatively minor (PGD = 0.9%; 0.64 Mya). Although the Pukerua Bay population forms a well-supported clade (81 bootstrap, 0.99 posterior probability), the level of genetic differentiation between the Pukerua Bay population and the two northeastern island populations (Castle Island PGD = 0.4%, 0.29 Mya; Mercury Islands PGD = 1.1%; 0.79 Mya) populations was not greater than that observed between the Castle Island and Mercury Islands populations (PGD = 1%; 0.71 Mya). A relatively high level of genetic differentiation was evident within both C. oliveri (PGD = 1.9%; 1.36 Mya) and C. townsi (PGD = 3.9%; 2.79 Mya).

Substantial geographic structuring is present within C. ornata (PGD = 4.1%; 2.93 Mya), with four well-supported clades evident (Fig. 3B). Clade 1 (70 bootstrap, 1.0 posterior probability; PGD = 1.9%; 1.36 Mya) contains populations from the Auckland region, the islands in the Hauraki Gulf (Mokohinau Islands, Hen and Chickens Islands, Little Barrier Island, Great Barrier Island), and Gisborne (Fig. 4B). Clade 2 (73 bootstrap, 1.0 posterior probability; PGD = 1.7%; 1.21 Mya) comprises populations from the Three Kings Islands and northern Northland (Fig. 4B). The Shimodaira–Hasegawa topology test clearly rejected the hypothesis that the Three Kings Islands population represents a distinct species (P = 0.002). Clade 3 (84 bootstrap, 1.0 posterior probability; PGD = 1.5%; 1.07 Mya) contains populations from across the lower North Island and a single population from Leigh, north of Auckland (Fig. 4B). Three subclades were evident within clade 3 (Fig. 3B), with the mean pairwise genetic distances between these subclades in the range 2.5–2.8% (1.79–2 Mya). The Poor Knights Islands (Aorangi) population represents the final clade (Clade 4) within C. ornata (Fig. 4B). The mean pairwise genetic distances between clades 1–3 ranges between 4.3–4.9% (3.07–3.50 Mya), but is significantly higher between clade 4 and the other three clades (PGD 8.7–9.8%; 6.21–7 Mya). It was not possible to conduct a topology test to examine the taxonomic status of the Poor Knights Islands C. ornata population since the genetic distinctiveness of this population was supported by the optimal ML tree (Fig. 3B).

DISCUSSION

Several contrasting phylogeographic patterns appear to exist within the genus Cyclodina. Subfossil evidence indicates that at least six Cyclodina species occurred sympatrically across the majority of the North Island during the Pleistocene (Worthy, 1987, 1991; Towns & Daugherty, 1994; Towns et al., 2001; BioWeb Herpetofauna Database, 2006). However, over the past 1–2 kyr, introduced mammals and anthropogenic impacts have modified reptile assemblages and resulted in dramatic declines in some species (Towns & Daugherty, 1994; Towns et al., 2001). Phylogeographic studies provide insight into how these disjunct and isolated distributional patterns were derived, and enable the level of population structuring in each species prior to decline to be inferred (Towns et al., 2001). Cyclodina species that remain widespread (C. aenea, C. ornata) display deep phylogeographic structure whereas, in northeastern island relic species (C. alani, C. oliveri, C. townsi), substantial divergence exists between populations on different island groups. By contrast, relatively shallow genetic divergences are evident between disjunct populations in both C. macgregori and C. whitakeri (North Island disjunct relics; Towns et al., 1985). We discuss the significance of these phylogeographic patterns, and examine the taxonomic implications of these findings.

Widespread species: Cyclodina aeneaandC. ornata

Cyclodina aenea and C. ornata are the two most widespread skink species in the North Island of New Zealand (Gill & Whitaker, 2001; Fig. 2A, B), with neither species exhibiting evidence of substantial recent range reduction (Towns et al., 1985; Towns & Daugherty, 1994; Towns et al., 2001). The two species occur sympatrically across the majority of their range, and display similar population structure, reproductive ecology, activity patterns (crepuscular), and habitat preferences (forest and scrub habitat) (Porter, 1987). However, C. aenea and C. ornata differ in morphology [e.g. C. ornata has a longer snout–vent length (SVL); Table 1] and some aspects of their behaviour and diet (Porter, 1987). Cyclodina aenea and C. ornata do not represent closely related sister species, with molecular evidence indicating that these two species diverged during the Miocene (our unpubl. data). Thus, it appears that C. aenea and C. ornata have independently converged on similar biology, ecology, and distributional patterns, providing an ideal opportunity to compare the phylogeography of these two species.

Although similar phylogeographic patterns are evident in both the C. aenea species complex and C. ornata, the depth and estimated timing of the divergences differs in each species (Fig. 3A, B). There are several patterns shared by both species: (1) relatively minor levels of phylogeographic structuring across the lower North Island; (2) substantial phylogeographic structure (i.e. multiple clades) in the Northland region; and (3) the significant divergence of the Poor Knights Islands populations.

Substantial phylogeographic structure is present in C. aenea, with one clade (clade 1) present in the lower North Island and four clades (clades 2–5) and two divergent populations (Dargaville, Whangarei) present in the Northland region (Fig. 4A). We found no evidence for the taxonomic distinctiveness of the Great Barrier Island populations as suggested by Hardy (1977). Phylogeographic structure and recent speciation in the Northland region has been documented in several taxa (Gleeson et al., 1999; Gardner et al., 2004; Spencer et al., 2006), including other skink species (Hare et al., 2008) and has usually been associated with the repeated connection and separation of populations as a result of sea level fluctuations during Pleistocene glacial cycles. However, no consistent patterns have emerged in regard to the location of these breaks. Our divergence time estimates indicate that phylogeographic structure within clades occurred during the Pleistocene, while those among clades originated in the late Pliocene–Pleistocene (Table 2). Cyclodina‘Te Paki’, the new species at the northern tip of Northland (Chapple et al., 2008b), appears to have diverged from C. aenea during the Miocene. Interestingly, more recent genetic divergence and speciation in this region of Northland has been documented in Kauri snails (Spencer et al., 2006).

Four clades are evident within C. ornata, with one clade (clade 4) representing a deeply divergent clade from the Poor Knights Islands (Fig. 3B). One C. ornata clade (clade 3) is present in the lower North Island, whereas another (clade 1) is distributed from the Hauraki Gulf region to East Cape (Fig. 4B). Although the Three Kings Islands populations were part of a clade (clade 2) that incorporated populations from the northern tip of Northland, there was no support for the taxonomic distinctiveness of these populations. Phylogeographic structure within C. ornata is deeper than that observed in C. aenea. The estimated divergences within clades appear to have occurred during the late Pliocene and Pleistocene, whereas the divergences among clades occurred during the Pliocene.

Volcanic activity in the Central Plateau region of the North Island during the Pleistocene (McDowall, 1996; Worthy & Holdaway, 2002) does not appear to have resulted in genetic breaks in C. aenea. However, there is a genetic break between C. ornata populations from either side of the Central Plateau (Fig. 4B). Thus, although the extensive deforestation that is believed to have resulted from volcanic eruptions (McDowall, 1996) might have restricted gene flow across the Central Plateau region in forest-dwelling taxa such as Cyclodina, evidence consistent with such events is only present in C. ornata. Indeed, it has been inferred from molecular data that volcanic eruptions resulted in repeated fragmentation of New Zealand short-tailed bat (Mystacina tuberculata) populations, with gene flow restored following reforestation (Lloyd, 2003a, b).

The Poor Knights Islands populations of both C. aenea and C. ornata represent deeply divergent lineages that potentially represent distinct species. Cyclodina aenea‘Poor Knights’ has recently been described as a new species (Chapple et al., 2008b), having diverged from C. aenea during the Miocene. Similarly, we estimate that the Poor Knights Islands population of ‘C. ornata’ diverged from C. ornata in the Miocene, providing strong support for this population representing a distinct species. Hardy (1977) suggested that the Poor Knights Islands ‘C. ornata’ was morphologically distinctive, and therefore further morphological work is required to assess its taxonomic status. The high incidence of endemic species on the Poor Knights Islands (Hitchmough, 1997; de Lange & Cameron, 1999) has generally been explained by the prolonged isolation (1–2 Myr) of this island group from the North Island mainland (Hayward, 1986, 1991). However, the estimated Miocene divergence of C. aenea‘Poor Knights’ and C. ornata‘Poor Knights’ indicates deeper divergences that pre-date the most recent land connection to the Poor Knights Islands.

North Island disjunct relics: Cyclodina macgregoriandC. whitakeri

The relatively minor level of phylogeographic structure present in C. macgregori and C. whitakeri provides an insight into the population structuring of these species prior to their recent declines. The shallow divergences present within both species indicates that gene flow was present between the disjunct populations until the late Pleistocene. This result supports the inference from subfossil evidence that both C. macgregori and C. whitakeri were continuously distributed across the North Island mainland prior to the arrival of humans and introduced mammals 1–2 kya (Worthy, 1987, 1991; BioWeb Herpetofauna Database, 2006). However, both species now have disjunct distributions with a limited number of populations on northeastern offshore islands and a single population in the Wellington region of the lower North Island (Fig. 2C, Table 1). There is strong evidence indicating that both species are unable to coexist with rats and/or mice (C. macgregori: Newman, 1994; C. whitakeri: Hoare et al., 2007), suggesting that introduced mammals are a likely cause for the declines (Towns & Daugherty, 1994; Towns, 1999; Towns et al., 2001). Both C. macgregori and C. whitakeri share similar activity patterns (nocturnal), habitat preferences (coastal forest and scrub), body size (SVL of approximately 100–110 mm), and have experienced similar declines (Table 1). Indeed, it has been noted previously that large nocturnal reptile species have been the most susceptible to introduced mammals, displaying the most dramatic declines (Towns & Daugherty, 1994; Towns et al., 2001).

Northeastern Island relics: Cyclodina alani, C. oliveri, andC. townsi

Subfossil evidence indicates that C. alani, C. oliveri, and C. townsi were widely distributed across the northern half of the North Island until 1–2 kya (Worthy, 1987, 1991; BioWeb Herpetofauna Database, 2006). None of these species remain on the North Island mainland, with their distributions restricted to northeastern offshore islands (Fig. 2C, D, Table 1). Although C. alani (SVL of approximately 142 mm) is considerably larger than C. oliveri and C. townsi (SVL of approximately 87–116 mm), the three species have similar activity patterns (nocturnal) and habitat preferences (coastal forest and scrub) (Table 1). All three species appear to be unable to coexist with introduced mammals (Towns, 1999). The phylogeographic patterns evident in C. oliveri and C. townsi are examined in detail elsewhere (Chapple et al., 2008a) but, in both species, divergences between populations on different island groups are estimated to have occurred during the late Pliocene and Pleistocene. Although only a limited number of samples were available for C. alani, there is evidence for similar deep divergences between populations on different island groups (Fig. 3B). The divergence between populations on the Mercury Islands and the Castle Island population is estimated to have occurred in the mid-Pleistocene, whereas the Matapia Island population appears to have diverged from both the Mercury Islands and Castle Island populations during the late Pliocene. Thus, it appears that the deep divergences between island groups were present in C. alani, C. oliveri, and C. townsi prior to their recent distributional declines.

Comparative phylogeography of the genusCyclodina

The phylogeographic patterns evident in Cyclodina species in the same biogeographic catergory (i.e. widespread species, North Island disjunct relics, northeastern island relics) are relatively consistent at a broad scale, but the patterns of genetic structuring appear to differ considerably between species in different biogeographic categories. This might be partly due to Cyclodina species within categories having more similar body size and habitat preferences compared to species in different biogeographic categories (Table 1). This result is intriguing because six Cyclodina species occurred sympatrically across the majority of the North Island until 1–2 kya (Towns & Daugherty, 1994; Towns et al., 2001). However, it is clear from our divergence time estimates that these phylogeographic patterns were created in the late Pliocene to mid-Pleistocene and significantly pre-date the impacts of humans and introduced mammals that have occurred over the past 1–2 kyr. Recent molecular studies of other New Zealand taxa have revealed deep divergences (i.e. Pliocene, Miocene) (Buckley et al., 2001; Arensburger, Simon & Holsinger, 2004; Chinn & Gemmell, 2004; Baker et al., 2005; Berry & Gleeson, 2005; Trewick & Morgan-Richards, 2005; Apte, Smith & Wallis, 2007; Hare et al., 2008), indicating that pre-Pleistocene processes have had a strong influence in shaping the evolution of the New Zealand biota.

Subfossil and genetic evidence indicates that every Cyclodina species (except the undescribed species within the C. aenea and C. ornata species complexes) is currently, or was previously (1–2 kya), continuously distributed across the Central Plateau region (Worthy, 1987, 1991; Towns & Daugherty, 1994; Towns et al., 2001; BioWeb Herpetofauna Database, 2006). By contrast, the distributions of Oligosoma species are restricted entirely to the north or entirely to the south of this region, with no species continuously distributed across the North Island (McCann, 1955; Bull & Whitaker, 1975; Towns et al., 1985; Gill & Whitaker, 2001). This is surprising because there is no evidence of phylogeographic structure across the Central Plateau region in any Cyclodina species apart from C. ornata (Fig. 4B). Interestingly, the Central Plateau region forms the boundary between two floristic biogeographic regions (Wardle, 1963; Connor, 2002) and therefore differences in the habitat requirements of Cyclodina and Oligosoma (Gill & Whitaker, 2001) might result in this region representing a major biogeographic barrier to Oligosoma. However, this pattern might also be a consequence of Cyclodina and Oligosoma differing in their response to the marine inundation of the lower North Island during the Pliocene (Rogers, 1989; King, 2000; Worthy & Holdaway, 2002).

Another interesting biogeographic contrast exists between Cyclodina and Oligosoma. Despite the presence of Cyclodina on the North Island since at least the Miocene, no evidence exists (current distributional data or fossil evidence) to indicate that any Cyclodina species occurs on the South Island (Gill & Whitaker, 2001; BioWeb Herpetofauna Database, 2006). However, the distribution of several Oligosoma species spans Cook Strait (O. infrapunctatum Boulenger, Oligosoma lineoocellatum Dumeril & Dumeril, Oligosoma nigriplantare polychroma, Oligosoma zelandicum Gray; Gill & Whitaker, 2001). Due to the repeated presence of a Cook Strait landbridge subsequent to the Pliocene (Worthy & Holdaway, 2002), there is evidence for recent (i.e. during the late Pleistocene) geneflow between populations either side of Cook Strait in O. zelandicum (O'Neill et al., 2008). The apparent inability of Cyclodina species to use such landbridges (or earlier Pliocene landbridges; Worthy & Holdaway, 2002) remains a largely unexplored biogeographic phenomenon.

ACKNOWLEDGEMENTS

We thank B. Kappers and A. Townsend for providing access to the Department of Conservation Herpetofauna database; L. Liggins and S. Greaves for assistance in the laboratory; and J. Moore for providing assistance in preparing the distributional maps. K. Britton, S. Keall, and R. Coory assisted in obtaining tissue samples from the National Frozen Tissue Collection and Te Papa. We especially thank L. Berry at the Allan Wilson Centre Genome Service. Funding for this project was provided by the Allan Wilson Centre for Molecular Ecology and Evolution, the Society for Research on Amphibians and Reptiles in New Zealand (SRARNZ), and the Victoria University of Wellington University Research Fund (VUW URF).

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