Eulamprus Research Articles

Maternal and additive genetic effects contribute to variation in offspring traits in a lizard

Evolutionary responses to selection require that traits have a heritable basis, yet maternal effects (the effect of a mother's phenotype on her offspring's phenotype) can have profound effects on evolutionary processes. It is therefore essential to understand how maternal effects contribute to phenotypic variation in offspring traits and test key assumptions of additive genetic variance in evolutionary models. We measured 5 traits linked to fitness in lizards (endurance, sprint speed, snout-vent length [SVL], mass, and growth rate) and estimated the contribution of additive genetic and maternal effects in explaining variation in these traits in the Eastern water skink (Eulamprus quoyii). We estimated parentage using 6 microsatellite DNA loci from lizards taking part in a mating experiment in large seminatural enclosures and used animal models to partition variance into additive genetic and maternal effects. We found that only endurance was significantly heritable (h(2) = 0.37, 95% credible interval = 0.18-0.50), whereas all other traits were either strongly influenced by maternal effects (mass, sprint speed, SVL, and captive growth rate) or were influenced by environmental variability (wild growth rate). Our study disentangles the relative contributions of additive genetic and maternal effects in contributing to variation in offspring phenotypes and suggests that little additive genetic variance exists for traits often assumed to be heritable. Although the heritability of phenotypic traits is essential in evolutionary models, our results also highlight the important role maternal effects have in explaining variation in phenotypes.

Multiple mating in a lizard increases fecundity but provides no evidence for genetic benefits

Multiple paternity is taxonomically widespread, yet the relative role of direct and indirect (genetic) fitness benefits in explaining the evolution of multiple mating is a topic of intense debate. We test whether female Eastern Water Skinks (Eulamprus quoyii) gain direct (fecundity) and/ or indirect genetic (increased offspring fitness) benefits through multiple mating. We maintained 216 (108 males and 108 females) E. quoyii in 6 large outdoor enclosures for a single breeding season before bringing gravid females into the lab to give birth. We classified female clutches as being singly or multiply sired using 6 polymorphic microsatellite DNA loci. To test whether females gain genetic benefits, we measured 5 fitness traits on offspring over their first active season and compared these traits between single paternity and multiple pater nity clutches. Contrary to predictions from genetic benefits models, offspring from multiple paternity and single paternity clutches did not differ significantly in snout–vent length, mass, growth rate, sprint speed, or endurance. Although multiple paternity and single paternity females did not differ significantly in body size, condition, or mass, multiple paternity females invested more heavily in reproduction when body size, mass, and condition were controlled, producing significantly more offspring compared with single paternity females. We suggest that polyandry in E. quoyii possibly evolved as a mechanism to ensure fertilization of ova, similar to what has been reported in some other taxa.

Population demography of an endangered lizard, the Blue Mountains Water Skink

BackgroundInformation on the age structure within populations of an endangered species can facilitate effective management. The Blue Mountains Water Skink (Eulamprus leuraensis) is a viviparous scincid lizard that is restricted to < 40 isolated montane swamps in south-eastern Australia. We used skeletochronology of phalanges (corroborated by mark-recapture data) to estimate ages of 222 individuals from 13 populations.ResultsThese lizards grow rapidly, from neonatal size (30 mm snout-vent length) to adult size (about 70 mm SVL) within two to three years. Fecundity is low (mean 2.9 offspring per litter) and is affected by maternal body length and age. Offspring quality may decline with maternal age, based upon captive-born neonates (older females gave birth to slower offspring). In contrast to its broadly sympatric (and abundant) congener E. tympanum, E. leuraensis is short-lived (maximum 6 years, vs 15 years for E. tympanum). Litter size and offspring size are similar in the two species, but female E. leuraensis reproduce annually whereas many E. tympanum produce litters biennially. Thus, a low survival rate (rather than delayed maturation or low annual fecundity) is the key reason why E. leuraensis is endangered. Our 13 populations exhibited similar growth rates and population age structures despite substantial variation in elevation, geographic location and swamp size. However, larger populations (based on a genetic estimate of effective population size) contained older lizards, and thus a wider variance in ages.ConclusionOur study suggests that low adult survival rates, as well as specialisation on a rare and fragmented habitat type (montane swamps) contribute to the endangered status of the Blue Mountains Water Skink.

Placentation in the eastern water skink (Eulamprus quoyii): a placentome-like structure in a lecithotrophic lizard

The eastern water skink (Eulamprus quoyii) has lecithotrophic embryos and was previously described as having a simple Type I chorioallantoic placenta. Indeed, it was the species upon which the definition of a Type I placenta was thought to be based, although we had cause to question that assumption. Hence we have described the morphology of the uterus of E.quoyii and found it to be more complex than previously supposed. The mesometrial pole of the uterus in E.quoyii displays a vessel-dense elliptical structure (the VDE) with columnar uterine epithelial cells. As pregnancy proceeds, the uterine epithelium near the mesometrial pole becomes folded and glands become hypertrophied, so that the morphology of VDE resembles that of a placentome, characteristic of Type III placentae. Unlike species with a Type III placenta, the apposing chorioallantoic membrane of E.quoyii is lined with squamous cells and interdigitates with the folded uterine epithelium. The remainder of the uterus is thin with a squamous uterine epithelium throughout pregnancy. Immunohistochemical localisation of blood vessels reveals a dense network of small capillaries directly beneath the folded epithelium of the VDE, while blood vessels are larger and sparser at the abembryonic pole of the uterus. Alkaline phosphatase (AP) activity is present in the uterine epithelium and sub-epithelial blood vessels in newly ovulated females. AP activity disappears from the epithelium between stages 27 and 29 of embryonic development and from the blood vessels after stage 34, but appears in the uterine glands at stage 35, where it remains until the end of pregnancy. Although the VDE is structurally similar to the placentomes found in other viviparous lizards, different distributions of AP activity in the uterus of E.quoyii and Pseudemoia spenceri suggest that the VDE may be functionally different from the placentome of the latter species. Our description of uterine morphology in E.quoyii provides evidence that, at least in some lineages, the evolution of a placentome may not occur in concert with the evolution of microlecithal eggs and obligate placentotrophy.

Sexual dimorphism and sexual selection in a montane scincid lizard (Eulamprus leuraensis)

AbstractSex‐based divergences in body sizes and/or shapes within a species imply that selective forces act differently on morphological features in males versus females. That prediction can be tested with data on the relationship between morphology and reproductive output in females, and between morphology and realized paternity (based on genetic assignment tests) in males. In a sample of 81 field‐collected adult Blue Mountains water skinks (Eulamprus leuraensis), males and females averaged similar overall body sizes (snout–vent lengths (SVLs)). Reproductive success (based on 105 progeny produced by the females) increased with SVL at similar rates in both sexes (as expected from the lack of sexual size dimorphism). Multiple paternity was common. Males had larger heads than females of the same body size, and (as predicted) reproductive success increased with relative head size in males but not in females. Males also had relatively longer limbs and shorter trunks than females, but we did not detect significant sex differences in selection on those traits. Reproductive success in both sexes was increased by relatively longer hind limbs. Our data clarify mating systems in this endangered species, and suggest that mating systems are diverse within the genus Eulamprus.

PREVALENCE OF SALMONELLA IN AUSTRALIAN REPTILES

From January 2007 until June 2008, 504 reptiles of four families and 57 species were examined for Salmonella by using cloacal or intestinal swabs. Salmonella was identified in 139 (28%) of the 504 animals tested. Of the 504 reptiles examined, 210 were captive and 294 were wild. Ninety-eight (47%) of the captive reptiles were shedding Salmonella at the time of sampling. In contrast, only 41 (14%) of the wild reptiles were shedding Salmonella. The higher prevalence of Salmonella in captive reptiles was statistically significant (P<0.0001). No Salmonella was found in 60 wild, freshwater chelonians or 48 wild southern water skinks (Eulamprus heatwolei). Our results suggest that some species of wild reptiles in Australia are not natural carriers of Salmonella and that diet and captivity may influence Salmonella excretion in other species.

Predicting the effects of climate change on reproductive fitness of an endangered montane lizard, Eulamprus leuraensis (Scincidae)

A shift in climatic conditions may directly modify critical organismal traits (such as reproductive output and offspring phenotypes), and experimental studies to document such direct effects thus may clarify the impacts of climate change on the species involved. The endangered Blue Mountains Water Skink (Eulamprus leuraensis) exhibits several traits predicted to imperil it under climate change: ectothermy, low reproductive output, specialisation to a restricted habitat type, montane endemicity, and a small geographic range. Congeneric species exhibit temperature-dependent sex determination, increasing potential sensitivity to climate change. We maintained wild-caught female lizards throughout pregnancy under thermal conditions simulating a shift in basking-time availability (3 vs 7 h/day) as might occur under climate change. Females with longer basking opportunities per day gave birth 2 weeks earlier, to slightly smaller offspring, that grew much faster in the first few weeks of life. Importantly, offspring sex ratios were not affected by maternal thermal regimes. Hence, some traits (e.g., offspring size, growth rates, dates of birth) are sensitive to ambient thermal conditions whereas other traits (e.g., offspring sex ratio and sprint speed) are not. On balance, the greatest threat to population persistence for E. leuraensis under climate change is likely to involve indirect effects mediated via habitat degradation (especially, drying-out of the hanging swamps) rather than direct thermal effects on lizard reproductive output or offspring phenotypes.

Plio‐Pleistocene diversification and genetic population structure of an endangered lizard (the Blue Mountains water skink, Eulamprus leuraensis) in south‐eastern Australia

AbstractAim Although climatic fluctuations occurred world‐wide during the Pleistocene, the severity of glacial and drought events – and hence their influence on animal and plant biogeography – differed among regions. Many Holarctic species were forced to warmer‐climate refugia during glacial periods, leaving the genetic signature of recent expansion and gene flow among modern‐day populations. Montane south‐eastern Australia experienced less extreme glaciation, but the effects of drier and colder climatic conditions over this period on biotic distributions, and hence on the present‐day genetic structure of animal and plant populations, are poorly known.Location South‐eastern Australia.Methods The endangered Blue Mountains water skink (Eulamprus leuraensis) is a viviparous lizard known from fewer than 40 isolated small swamps at 560–1060 m elevation in south‐eastern Australia. We conducted molecular phylogenetic, dating and population genetics analyses using the mitochondrial NADH dehydrogenase 4 (ND4) of 224 individuals of E. leuraensis sampled across the species’ distribution.Results Ancient divergences in haplotype groups between lizards from the Blue Mountains and the Newnes Plateau, and strong genetic differences, even between swamps separated by only a few kilometres, suggest that the species has persisted as a series of relatively isolated populations within its current distribution for about a million years. Presumably, habitat patches similar to current‐day swamps persisted throughout glacial–interglacial cycles in this region, allowing the development of high levels of genetic structuring within and among present‐day populations.Main conclusions Our results suggest that less extreme glacial conditions occurred in the Southern Hemisphere compared with the Northern Hemisphere, allowing cold‐adapted species (such as E. leuraensis) to persist in montane areas. However, additional studies are needed before we can assemble a comprehensive view of the impact of Pleistocene climatic variation on the phylogeography of Southern Hemisphere taxa.

A review of the genus Tropidophorus (Squamata, Scincidae) from Vietnam with new species records and additional data on natural history

At present, eight species of the water skink genus Tropidophorus are recognized from Vietnam. We provide expanded species descriptions based on new collections and new distributional and natural history data of all Vietnamese water skinks. In addition, an identification key to the species of Tropidophorus from the Indochinese Peninsula is presented. (© 2010 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim)

Restricted dispersal and genetic diversity in populations of an endangered montane lizard (Eulamprus leuraensis, Scincidae)

Many alpine species are under threat from global climate change, as their geographic ranges become increasingly fragmented and unsuitable. Understanding rates and determinants of gene flow among such fragmented populations, over historical as well as recent timescales, can help to identify populations under threat. It is also important to clarify the degree to which loss of local populations reduces overall genetic diversity within the taxon. The endangered Blue Mountains Water Skink (Eulamprus leuraensis) is restricted to <40 small swamps in montane south-eastern Australia. Our analyses of seven microsatellite loci of 241 animals from 13 populations show strong geographic structure, with major genetic divergence even between populations separated by <0.5 km. Dispersal between populations is scarce, and appears to involve mostly males. Our analyses suggest potential recent bottleneck events in all the identified populations, and lower genetic diversity and population size parameter at lower-elevation sites than at higher-elevation sites. Management of this endangered taxon thus needs to treat most populations separately, because of their genetic distinctiveness and low rates of genetic exchange.

Modelling life history strategies with capture-recapture data: Evolutionary demography of the water skink Eulamprus tympanum

Matrix population models, elasticity analysis and loop analysis can potentially provide powerful techniques for the analysis of life histories. Data from a capture–recapture study on a population of southern highland water skinks (Eulamprus tympanum) were used to construct a matrix population model. Errors in elasticities were calculated by using the parametric bootstrap technique. Elasticity and loop analyses were then conducted to identify the life history stages most important to fitness. The same techniques were used to investigate the relative importance of fast versus slow growth, and rapid versus delayed reproduction. Mature water skinks were long-lived, but there was high immature mortality. The most sensitive life history stage was the subadult stage. It is suggested that life history evolution in E. tympanum may be strongly affected by predation, particularly by birds. Because our population declined over the study, slow growth and delayed reproduction were the optimal life history strategies over this period. Although the techniques of evolutionary demography provide a powerful approach for the analysis of life histories, there are formidable logistical obstacles in gathering enough high-quality data for robust estimates of the critical parameters.

Chemical mediation of reciprocal mother–offspring recognition in the Southern Water Skink (Eulamprus heatwolei)

Abstract Kin recognition has been demonstrated to play an important role in the social structure of a wide range of animals. Most studies to date have examined parent–offspring recognition only in species that provide offspring with direct parental care, however, there are several advantages to parent–offspring recognition even in the absence of direct parental care. In this study we investigated reciprocal mother–offspring recognition in the Australian scincid lizard Eulamprus heatwolei, a species that does not show direct parental care. We examined whether neonates could discriminate between their mothers and unrelated females, and whether females could discriminate between their offspring and unrelated neonates, via chemical cues, using retreat site selection experiments. We conducted trials when neonates were 1 and 4 weeks old to investigate whether responses are maintained as neonates age. We found that both neonates and mothers could discriminate between related and unrelated individuals when neonates were 1 week old. Mothers were more likely to take refuge under tiles treated with the odours of their own offspring, while neonates spent less time in areas treated with the odours of unrelated females. At 4 weeks of age, mothers no longer exhibited discriminatory behaviour between their offspring and unrelated neonates, while neonates were more likely to associate with the odour of any female over the odourless control. We hypothesize that reciprocal mother–offspring recognition in E. heatwolei reduces interference competition between mothers and their offspring and also may be important in habitat selection and territory establishment.

Remarkably different phylogeographic structure in two closely related lizard species in a zone of sympatry in south‐eastern Australia

AbstractPhylogeographic structure is a product of a species' life history and dispersal patterns, geographic history, climatic history and chance. Comparative phylogeography, using carefully chosen model species, can highlight the relative contribution of each of these factors and identify common processes affecting communities. In this study we compare and contrast fine‐scale phylogeographic patterns in two ground‐dwelling species of water skink, Eulamprus heatwolei and Eulamprus tympanum, from the biogeographically well‐characterized Tallaganda region in south‐eastern Australia, and compare them against data from a number of invertebrate species from the same region. Using variation in mitochondrial sequence, we have uncovered dramatically different biogeographic histories for the two species, despite their marked behavioural and morphological similarity. Eulamprus tympanum shows an average corrected sequence divergence of 0.014 and patterns of geographic variation in haplotypes consistent with historical vegetational changes resulting from past glaciation cycles. In contrast, E. heatwolei shows an average divergence of only 0.0075, and geographic structure that reflects a recent and rapid colonization, perhaps following an ice age local extinction. These two contrasting patterns of variation have also been identified in invertebrate taxa as disparate as collembolans and spiders; these species show either deep structure, associated with local persistence, or little variation of structure, which we attribute to recent extinction and re‐colonization. We argue that historical persistence versus extinction is a consequence of (often minor) differences in lifestyle and local habitat preference.

Do operational sex ratios influence sex allocation in viviparous lizards with temperature-dependent sex determination?

Under certain environmental situations, selection may favour the ability of females to adjust the sex ratio of their offspring. Two recent studies have suggested that viviparous scincid lizards can modify the sex ratio of the offspring they produce in response to the operational sex ratio (OSR). Both of the species in question belong to genera that have also recently been shown to exhibit temperature-dependent sex determination (TSD). Here we test whether pregnant montane water skinks (Eulamprus tympanum) utilise TSD to select offspring sex in response to population wide imbalances in the OSR, by means of active thermoregulation. We use a combination of laboratory and field-based experiments, and conduct the first field-based test of this hypothesis by maintaining females in outdoor enclosures of varying OSR treatments throughout pregnancy. Although maternal body temperature during pregnancy was influenced by OSR, the variation in temperature was not great enough to affect litter sex ratios or any other phenotypic traits of the offspring.

Phylogeny and biogeography of water skinks of the genus Tropidophorus (Reptilia: Scincidae): a molecular approach

Phylogenetic relationships of the Oriental semiaquatic lygosomine skinks of the genus Tropidophorus were inferred from 1219 base positions of mitochondrial 12S and 16S rRNA genes. Results of the phylogenetic analyses incorporating data for representatives of other lygosomine genera indicated that the basal phylogenetic split within Tropidophorus separated a clade of continental Indochinese species exclusive of T. cocincinensis and T. microlepis from one comprising T. cocincinensis, T. microlepis and species from Borneo, Sulawesi and the Philippines. Of the latter group, the two continental species form the sister taxon to a clade comprising the island species. Diversification among species in Indochina and among Borneo, the Philippines and Sulawesi was likely concentrated in the Miocene, with no apparent dispersal among these regions during the Pleistocene. The body depression recognized in several Indochinese species is likely to have occurred twice in parallel as an adaptation to saxicolous habitats.

The ecology of a host-parasite relationship: Haemogregarines &amp; the eastern water skink, Eulamprus quoyii

The ecology of a host-parasite relationship: Haemogregarines &amp; the eastern water skink, Eulamprus quoyii

Male southern water skinks (Eulamprus heatwolei) use both visual and chemical cues to detect female sexual receptivity

A wide range of organisms use chemical and visual cues in mate attraction and courtship; however, chemical discrimination relevant to reproduction and the interplay between these two types of communication are poorly understood in reptiles. We experimentally tested the ability of male Eulamprus heatwolei, a scincoid lizard, to discriminate between sexually receptive and non-receptive females in two ways. First, we conducted 155 staged encounters between males and females over 29 days to determine the start and the duration of the female receptive period based on the date of copulations. These data suggest that the receptive period lasted for approximately 7 days in late October under controlled laboratory conditions. We also recorded 6,330 individual male and female behaviours during these trials to evaluate the frequency of female courtship and rejection behaviours and the intensity of male courtship behaviour. Female courtship increased sharply during the receptive period and then diminished. The disparity between female courtship behaviours and female rejection behaviours was greatest during the receptive period. Male courtship intensity increased sharply prior to the receptive period, peaked during the receptive period and thereafter declined rapidly. To determine if males were using visual cues, chemical cues or both from females, we conducted an experiment during and after the receptive period wherein male lizards were presented with a choice of two retreat sites treated either with the odour of large sexually receptive females, odour of small sexually non-receptive females or no odour (control). Males preferred the scent of females over the odourless control, and analysis using a special form of a generalized linear model, the Bradley–Terry model, showed a clear order of retreat site preferences, with large sexually receptive females favoured over small non-receptive females over the odourless control. We speculate that males use vision to find females and then use their chemosensory ability to chemically evaluate female sexual receptivity once the pair are in close proximity.

SEXUAL DIMORPHISM IN BODY SHAPE WITHOUT SEXUAL DIMORPHISM IN BODY SIZE IN WATER SKINKS (EULAMPRUS QUOYII)

Sexual dimorphism in body size is often accompanied by shape dimorphism. Shape dimorphism may be selected directly, or may be an indirect result of selection for size dimorphism. To determine whether shape differences are likely to have been directly influenced by selection, the indirect effects of size dimorphism on shape can be removed statistically, the approach of most previous studies, or, alternatively, we can examine the patterns of shape dimorphism in species that are not size dimorphic. Here I describe sexual shape dimorphism in adults and neonates of a lizard that is not dimorphic in body length, the eastern water skink (Eulamprus quoyii). In this species, snout–vent length is not significantly different between adult or neonate males and females, but there are significant shape differences between sexes in both adults and neonates. For a given body length, adult males have wider heads, longer limbs, shorter trunk length (the distance between the forelimb and the hindlimb), and greater mass than females. In addition, head width, forelimb length and mass increase significantly more rapidly with body length in adult males than in females, whereas the rate of change of hindlimb length and trunk length with length is not significantly different in males and females. The shape of the body is more similar in neonates than adults, but female neonates have significantly longer trunks than males. The intersexual shape difference in neonate E. quoyii suggests that, although growth rate differences among body parts are the main source of differences in shape between adults, the difference between male and female interlimb lengths is present initially. Shape differences present at birth that are preserved until adulthood are less common than growth differences as a source of adult shape differences. The intersexual shape differences among adult E. quoyii are similar to those reported for species that are sexually size dimorphic, suggesting that selective forces have influenced body shape in similar ways in both size dimorphic and nondimorphic species, and that allometric relationships alone may not be responsible for shape differences between males and females in size dimorphic species.

How do water skinks avoid shelters already occupied by other lizards?

Animals rely on a wide range of sensory modalities to obtain information about their environment, and to determine the most appropriate behavioural response for a give situation. Scincid lizards use both chemosensory and visual cues in tasks such as mate location, shelter-site selection, and predator evasion. Published literature has focused primarily on the use of chemosensory information by these lizards, but our experiments reveal an alternative scenario. Water skinks (Eulamprus heatwolei) are sympatric with larger black rock skinks (Egernia saxatilis) in southeastern Australia, and use similar long-term retreat-sites. However, Eulamprus avoid shelter-sites occupied by Egernia because of the risk of attack and injury. We conducted laboratory trials to clarify the kinds of information used by Eulamprus to avoid already-occupied shelters. In the field, shelter-sites might provide three types of information about prior occupancy: either scent deposited by a previously present Egernia; evidence of the current presence of an Egernia, perhaps involving visual, chemical, and/or auditory information; or a direct behavioural interaction with a resident lizard (potentially involving an attack). In our trials, Eulamprus based their shelter-site avoidance only on direct interactions. Thus, Eulamprus reacted strongly to Egernia with which they were able to interact physically, but not to either Egernia scent deposits, or a (caged) Egernia with which they could not physically interact. The behaviour of the resident was critical, in that Eulamprus fled from the crevice in response to bites, movements, or open-mouth displays by the resident Egernia. We suggest that Eulamprus base their shelter-site choices on the presence of an actual resident animal rather than more indirect cues (such as scent), because only a direct encounter provides reliable information about the magnitude of threat associated with crevice occupancy.

Exploratory and antipredator behaviours differ between territorial and nonterritorial male lizards

Alternative territorial tactics may be part of a broader behavioural tendency that can influence the expression of other behavioural traits. We compared the exploratory and predator avoidance behaviours of territorial and floater male water skinks, Eulamprus heatwolei, to identify whether these alternative behavioural tactics are part of a broader behavioural dichotomy. Floater and territorial males differed in their tendencies to explore novel habitats. Floaters spent less time in the refuge, moved further and ate more mealworms when placed in a novel enclosure, suggesting that floaters were less wary of the novel environment and had greater exploratory tendencies. Predator avoidance behaviours also differed between the two groups of males. Territorial lizards were less likely to retreat to a refuge site during a simulated predator attack, returned faster to a basking site after this attack and as a result had a smaller net reduction in preattack body temperature. These results may be attributed to the trade-off that territorial lizards face between territorial defence and antipredator behaviour, which floaters do not experience. Our results suggest that territorial tactics may be part of a broader behavioural tendency that can influence the expression and evolution of other seemingly unrelated traits.