Jane Melville

Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota

The integration of phylogenetics, phylogeography and palaeoenvironmental studies is providing major insights into the historical forces that have shaped the Earths biomes. Yet our present view is biased towards arctic and temperate/tropical forest regions, with very little focus on the extensive arid regions of the planet. The Australian arid zone is one of the largest desert landform systems in the world, with a unique, diverse and relatively well-studied biota. With foci on palaeoenvironmental and molecular data, we here review what is known about the assembly and maintenance of this biome in the context of its physical history, and in comparison with other mesic biomes. Aridification of Australia began in the Mid-Miocene, around 15 million years, but fully arid landforms in central Australia appeared much later, around 1-4 million years. Dated molecular phylogenies of diverse taxa show the deepest divergences of arid-adapted taxa from the Mid-Miocene, consistent with the onset of desiccation. There is evidence of arid-adapted taxa evolving from mesic-adapted ancestors, and also of speciation within the arid zone. There is no evidence for an increase in speciation rate during the Pleistocene, and most arid-zone species lineages date to the Pliocene or earlier. The last 0.8 million years have seen major fluctuations of the arid zone, with large areas covered by mobile sand dunes during glacial maxima. Some large, vagile taxa show patterns of recent expansion and migration throughout the arid zone, in parallel with the ice sheet-imposed range shifts in Northern Hemisphere taxa. Yet other taxa show high lineage diversity and strong phylogeographical structure, indicating persistence in multiple localised refugia over several glacial maxima. Similar to the Northern Hemisphere, Pleistocene range shifts have produced suture zones, creating the opportunity for diversification and speciation through hybridisation, polyploidy and parthenogenesis. This review highlights the opportunities that development of arid conditions provides for rapid and diverse evolutionary radiations, and re-enforces the emerging view that Pleistocene environmental change can have diverse impacts on genetic structure and diversity in different biomes. There is a clear need for more detailed and targeted phylogeographical studies of Australias arid biota and we suggest a framework and a set of a priori hypotheses by which to proceed.

The Role of Geography and Ecological Opportunity in the Diversification of Day Geckos (Phelsuma)

We examine the effects of ecological opportunity and geographic area on rates of species accumulation and morphological evolution following archipelago colonization in day geckos (genus Phelsuma) in the Indian Ocean. Using a newly generated molecular phylogeny for the genus, we present evidence that these geckos likely originated on Madagascar, whereas colonization of three archipelagos in the Indian Ocean, the Seychelles, Mascarene, and Comoros Islands has produced three independent monophyletic radiations. We find that rates of species accumulation are not elevated following colonization but are roughly equivalent on all three isolated archipelagos and on the larger island of Madagascar. However, rates of species accumulation have slowed through time on Madagascar. Rates of morphological evolution are higher in both the Mascarene and Seychelles archipelagos compared to rates on Madagascar. This negative relationship between rate of morphological evolution and island area suggests that ecological opportunity is an important factor in diversification of day gecko species.

Molecular phylogenetic evidence for ancient divergence of lizard taxa on either side of Wallace's Line.

Wallaces Line, separating the terrestrial faunas of South East Asia from the Australia-New Guinea region, is the most prominent and well-studied biogeographical division in the world. Phylogenetically distinct subgroups of major animal and plant groups have been documented on either side of Wallaces Line since it was first proposed in 1859. Despite its importance, the temporal history of fragmentation across this line is virtually unknown and the geological foundation has rarely been discussed. Using molecular phylogenetics and dating techniques, we show that the split between taxa in the South East Asian and the Australian-New Guinean geological regions occurred during the Late Jurassic to Early Cretaceous in two independent lizard clades. This estimate is compatible with the hypothesis of rifting Gondwanan continental fragments during the Mesozoic and strongly rejects the hypothetical origin of various members of the Australian-New Guinean herpetofauna as relatively recent invasions from South East Asia. Our finding suggests an ancient fragmentation of lizard taxa on either side of Wallaces Line and provides further evidence that the composition of modern global communities has been significantly affected by rifting and accretion of Gondwanan continental plates during the Middle to Late Mesozoic.

EVIDENCE OF CONSTRAINED PHENOTYPIC EVOLUTION IN A CRYPTIC SPECIES COMPLEX OF AGAMID LIZARDS

Lineages that exhibit little morphological change over time provide a unique opportunity to explore whether nonadaptive or adaptive processes explain the conservation of morphology over evolutionary time scales. We provide the most comprehensive evaluation to date of the evolutionary processes leading to morphological similarity among species in a cryptic species complex, incorporating two agamid lizard species (Diporiphora magna and D. bilineata). Phylogenetic analysis of mitochondrial (ND2) and nuclear (RAG‐1) gene regions revealed the existence of eight deeply divergent clades. Analysis of morphological data confirmed the presence of cryptic species among these clades. Alternative evolutionary hypotheses for the morphological similarity of species were tested using a combination of phylogenetic, morphological, and ecological data. Likelihood model testing of morphological data suggested a history of constrained phenotypic evolution where lineages have a tendency to return to their medial state, whereas ecological data showed support for both Brownian motion and constrained evolution. Thus, there was an overriding signature of constrained evolution influencing morphological divergence between clades. Our study illustrates the utility of using a combination of phylogenetic, morphological, and ecological data to investigate evolutionary mechanisms maintaining cryptic species.

Correlates of active body temperatures and microhabitat occupation in nine species of central Australian agamid lizards

Body temperatures of active lizards and their correspondence with microhabitat occupation were studied for nine species of agamid lizards in the central Australian arid zone. Thermoregulatory behaviour was also documented using several measures, such as the use of shade and perch height. The effects of thermal environment on lizard habitat occupation were hypothesized to be significant, because desert regions experience daily and seasonal extremes of temperature that are well in excess of a lizard’s preferred temperature range. All species, except Ctenophorus isolepis and Diporiphora winneckei, were found to have body temperatures that corresponded closely to ground and surface temperatures. Thermoregulatory behaviour was also found to be important throughout a lizard’s daily activity; all study species, other than Ctenophorus isolepis, were found to increase their perch height in the middle of the day. Ctenophorus isolepis was shown to be a strictly terrestrial species that uses the shade of spinifex in its thermoregulatory behaviour. Species exhibited a non-random selection of microhabitats and a preference for a particular set of thermal and structural factors. In this study, it was shown that structural factors were particularly important in microhabitat occupation. Thermal factors accounted for a smaller proportion of variance in microhabitat occupation, but still played a considerable role in the microhabitat use in central Australian agamids.

Evolutionary origins and diversification of dragon lizards in Australia's tropical savannas

Australias monsoonal tropics are dominated by the largest and least modified savanna woodlands in the world, and they are globally significant for their high biodiversity and regional endemism. Despite this, there have been very few molecular studies of the evolutionary origins and diversification of vertebrates in this region. The semi-arboreal dragon lizards of Lophognathus and Amphibolurus are widely distributed in the savanna and dry sclerophyll woodlands of Australasia, including the monsoon tropics. We sequenced a ~1400 bp region of mitochondrial DNA and a ~1400 bp nuclear gene (RAG1) to investigate the phylogenetic relationships and phylogeographic structuring of all seven species of Lophognathus and Amphibolurus. Our analyses show that there is a higher level of species and generic diversity in the monsoon tropics than previously thought, and a full morphological review and taxonomic revision of these genera is required. Relaxed molecular clock analyses indicate that species across both genera originated in the late Miocene and early Pliocene, with significant phylogeographic structure within species. We did not find any evidence that the monsoon tropics species were a monophyletic group that had diversified within the region; instead Amphibolurus and Lophognathus represent at least three independent evolutionary colonizations of the monsoon tropics. It is probable that the origins and phylogeographic patterns of the northern Lophognathus species have evolved under the climatic influence of the Australian monsoon, rather than being either an ancient Gondwanan lineage that pre-dates the monsoon or the result of a more recent dispersal event across Wallaces Line.

Historical biogeography, phylogenetic relationships and intraspecific diversity of agamid lizards in the Central Asian deserts of Kazakhstan and Uzbekistan

The Central Asian agamid lizards are ecologically and morphologically diverse, occurring across a broad range of desert environments in this biogeographically important region. It is probable that past climatic shifts have significantly influenced the diversification patterns and distributions of the agamid lizards of this region. To assess this within a phylogenetic framework we sequenced a approximately 1200 bp region of mitochondrial DNA and a approximately 1200 bp nuclear gene (RAG-1), incorporating both inter- and intraspecific sampling across Central Asian agamids. Our topology and divergence time estimates support an Eocene origin of the Agaminae subfamily on the Indian subcontinent, coinciding with the collision of India into Eurasia. The onset of aridification in Central Asia during the Late Oligocene, resulting from the retreat of the Paratethys Sea and the intensified uplift of the Tibetan-Himalayan complex, probably played an important role in the diversification of Phrynocephalus, one of the three genera studied. Intensification of aridity and geologic events in the Plio-Pleistocene and Quaternary glacial cycling probably had a significant influence on intraspecific diversification patterns within Phrynocephalus.

Evolutionary correlations between escape behaviour and performance ability in eight species of snow skinks (Niveoscincus: Lygosominae) from Tasmania

Three locomotor modes were examined (sprinting, jumping and climbing) in eight species of skinks: seven Niveoscincus spp. and Pseudemoia entrecasteauxii. These species formed four distinct ecological types: ground-dwelling, arboreal, heath/rock dwelling, and saxicolous. Significant behavioural preferences for particular escape modes in the field were found, which reflected the performance capabilities at an animal in the laboratory. This study used both non-phylogenetic and evolutionary based analyses to demonstrate that species occupying different microhabitats and using different escape tactics exhibit corresponding differences in performance abilities. Four Niveoscincus species are specialized in performance abilities and behavioural responses (N. greeni, N. ocellatus, N. pretiosus, N. orocryptus) by excelling in some performance abilities but having behavioural restrictions at attemping other locomotor modes. Only N. microlepidotus and N. orocryptus used escape tactics opportunistically; these species possess a suite of behavioural responses that may reflect the wide range of microhabitats they occupy. Ground-dwelling species N. metallicus, N. coventryi and Pseudemoia entrecasteauxii performed poorly at all performance abilities and seemed to have biomechanical limitations, rather than behavioural restrictions, on locomotor mode. Thus, when making interspecific comparisons, the behaviour of an animal needs to be considered before appropriate performance measures are selected. Phylogenetic analyses demonstrate that escape tactics and performance abilities have co-evolved in Niveoscincus, with an evolutionary trend towards behavioural and locomotor specialization.

Daily and Seasonal Activity Patterns in Two Species of High Altitude Skink, Niveoscincus microlepidotus and N. metallicus, from Tasmania

-We studied the activity patterns of two species of viviparous lizards co-occurring in a harsh sub-alpine environment. Activity patterns were studied over the active period, October to March, to investigate differences between an alpine specialist species, Niveoscincus microlepidotus, and a lowland generalist species, N. metallicus, at its altitudinal limit. Distinct differences were found in emergence and retreat times, behavior during the day, activity between the seasons, and total activity over the summer period. Loglinear modeling clearly showed a relationship between sex, season and the behavior of the lizards. Niveoscincus microlepidotus exhibited more variable behavior than N. metallicus, with a capacity to shift from bimodal to unimodal diel activity. Diel and seasonal activity in N. microlepidotus was greatly extended, largely through the use of thigmothermy to supplement shuttling heliothermy. Activity patterns in heliothermic lizards are often determined by climate and weather, and particularly by contemporary levels of insolation (Avery, 1978; House et al., 1980). Because the body temperature of an ectotherm is a complex function of its biophysical environment (Grant and Dunham, 1988), thermoregulating lizards are constrained to occupy specific thermal activity windows. A lizard that can be active for longer periods will ultimately have more available energy. Assuming that food is readily available, daily energy assimilation should increase with activity time, because the rates of digestion and assimilation are temperature dependent (Van Damme et al., 1991) and are maximized at or near active body temperatures (Avery et al., 1982). At high altitudes lizards may be inactive for more than half the year. During this time they must survive on stored energy, particularly lipids, and these energy stores, built up over the warmer months, must be adequate for the duration of hibernation (Adolph and Porter, 1993). Consequently, an increased activity window during summer months, both on a diel and seasonal basis, may increase survivorship over the winter period. Time is therefore an important resource, and temporal partitioning may consequently be of great adaptive importance to species of lizards found at high altitudes (Simon and Middendorf, 1976; Toft, 1985). The two species chosen for this study were Niveoscincus microlepidotus, an alpine specialist, and N. metallicus, a species primarily associated with more temperate habitats; both are viviparous. Mating in N. microlepidotus may occur at any point during summer (DecemberFebruary) (M. Olsson pers. comm.). Females that mate early in the season usually carry their embryos through hibernation until the following spring; those that mate towards the end of summer ovulate in spring (September) after carar er months, must be adequate for the dution of hibernation (Adolph and Porter, 1993). sequently, an increas d activity window ring sum er months, both on a diel and seaal basis, may increas survivorship over the 29 This content downloaded from 207.46.13.101 on Sat, 08 Oct 2016 06:08:15 UTC All use subject to http://about.jstor.org/terms J. MELVILLE AND R. SWAIN rying sperm through winter. In N. metallicus young are born in late summer, mating occurs in late autumn and females carry sperm through winter and ovulate in spring; some females mate again in September (Swain and Jones, 1994; Jones and Swain, in press). Our study was carried out at the tree line on Mt Wellington, southern Tasmania, where the two species co-occur. The site represents the upper and lower altitudinal limits on the mountain of N. metallicus and N. microlepidotus respectively. The climate is sub-alpine and, although strongly seasonal, rapid and substantial diel changes frequently occur. Snow may fall in any month of the year, but is most common during winter when the lizards hibernate. The active period for reptiles at this site is from spring (late September) to autumn (late April) (unpubl. data). High altitude Scelporus jarrovi exhibit both unimodal and bimodal activity patterns in response to variations in their thermal environment (Beuchat, 1989). Our study was undertaken to see if this occurs also in N. microlepidotus and N. metallicus, and to determine whether any differences in temporal partitioning that might exist between these species were relevant to their altitudinal distributions. MATERIALS AND METHODS The Study Sites.-Two adjacent but separate sites were chosen for this study to take account of clear differences in microhabitat preferences for the two species (unpubl. data). The total area was approximately 80 m x 50 m and the proximity of the sites meant that it was a matter of only a few steps to move from one to the other to make observations. The sites were within the sub-alpine to alpine transition zone at an altitude of 1080 m, on the eastern face of Mt. Wellington. Rainfall at the location is high, frosts are frequent, and glazing storms occur throughout the year, but snow cover is usually restricted to winter and early spring. The area consists of a mosaic of three distinct macrohabitats: subalpine woodland, alpine heath, and boulder fields. Niveoscincus metallicus were observed in open sub-alpine woodland which is their preferred habitat at this altitude; densities are in the range 10-20 in a 10 x 10 m square. Sub-alpine woodlands are typical of dolerite-capped mountains in the east of Tasmania and, on Mt. Wellington, this community type occurs between 1000 and 1100 m. Canopy coverage is <30%, allowing a vigorous understorey, up to about 1.5 m in height. In places litter layers, composed mainly of eucalypt debris, accumulate up to 30 cm in depth. Maximum canopy height is 10 m and is dominated by the snow gum, Eucalyptus coccifera. Alpine heaths occur in association with poorly drained, acidic peat soils. Trees are absent and the vegetation height does not exceed 1.5 m. The ground cover is low and dense and numerous alpine plant species are present. Low numbers of both species occur in this habitat, which was not utilised for this study. Niveoscincus microlepidotus were observed in a dolerite boulder field. In this habitat, vegetation is restricted to encrusting lichen and mosses on the surface of boulders, which range in diameter from 0.5-8 m. Lizard densities of 25-35 individuals 100 m-2 were present. Field Observations.-Early in spring, twelve individuals (4 male, 4 female, 4 juvenile) of N. microlepidotus and nine individuals (3 male, 3 female, 3 juvenile) of N. metallicus were captured, sexed, and tagged by a small (2 mm x 2 mm) piece of colored tape stuck to the dorsal surface. As an extra identification measure, each animal was also given a unique toe-clip. Weekly visits were paid to the study site to check on the condition of the tags; when necessary animals were recaptured and the tag replaced. Sexing was achieved by eversion of the hemipenes in males and by gentle palpitation to locate developing ggs or embryos in the females. In spring all female N. microlepidotus observed carried advanced embryos and the female N. metallicus all contained very early embryos. In summer, two of the four N. microlepidotus had well developed embryos, while all of the female N. metallicus were in this condition. In the autumn sample one N. microlepidotus was pregnant and all three N. metallicus were post partum. The 21 marked individuals were observed over a period of three days in each of late spring, mid-summer and autumn. Daily patterns of acivity were recorded for both species. Particular care was given to choosing days for observations in which similar weather conditions prevailed; warm sunny days with little cloud cover were chosen in order to minimize differences in behavior associated with heavy cloud, rain squalls or snow showers. Observations commenced at 0630 h (Local Summer Time), prior to emergence, and were continued until half an hour after the final retreat each day. At five minute intervals a record was made of all lizards visible and the activity of each lizard. Observations took approximately 5 min, after which the observer moved to the adjacent site; observations continued throughout the day and all were carried out by the same person (JM). Activity was recorded using the following behavior categories: overt basking-sitting in the full sun for extended periods of usually more than five minutes; body flattened, often with the legs held back against the side of the body; 30 This content downloaded from 207.46.13.101 on Sat, 08 Oct 2016 06:08:15 UTC All use subject to http://about.jstor.org/terms ACTIVITY PATTERNS IN ALPINE SKINKS TABLE 1. Range of emergence and retreat times and air temperatures for Niveoscincus microlepidotus and N. metallicus. N values identify the number of times marked individuals (12 N. microlepidotus, 9 N. metallicus) were observed in a 3 day observation period. All times are Local Summer Time.

Molecular patterns of introgression in a classic hybrid zone between the Australian tree frogs, Litoria ewingii and L. paraewingi: evidence of a tension zone

Hybrid zones provide a rare opportunity to explore the processes involved in reproductive isolation and speciation. The southern hybrid zone between the southeastern Australian tree frogs Litoria ewingii and L. paraewingi has been comprehensively studied over the last 40 years, primarily using reproductive compatibility experiments and male advertisement calls. We used mitochondrial DNA (mtDNA) and eight nuclear microsatellite markers to characterize this hybrid zone along a historically studied transect and to test various dispersal‐dependent and dispersal‐independent hybrid zone models. The species are genetically distinct and the level of hybridization within the contact zone is low, with the majority of admixed individuals representing later‐generation hybrids. Based on previous experimental genetic compatibility studies, we predicted that hybrids with L. paraewingi mtDNA would be more frequent than hybrids with L. ewingii mtDNA. Surprisingly, a greater proportion of the identified hybrids had L. ewingii mtDNA. Geographical cline analyses showed a sharp transition in allele frequencies across the transect, and both the mtDNA and microsatellite data showed concordant cline centres, but were best supported by a model that allowed width to vary. Overall, the L. ewingii–L. paraewingi hybrid zone is best characterized as a tension zone, due to the narrow cline width, concordant genetic clines and low levels of hybridization.