Herpetology Notes, volume 14: 251-255 (2021) (published online on 01 February 2021)

Melanism in the eastern blue-tongued lizard Tiliqua scincoides (Squamata: Scincidae) from south-eastern Australia

Jules E. Farquhar1

Animals display extraordinary variety in Clusella-Trullas et al., 2007). Broadly, the TMH predicts integumentary colouration, both within and among that dark phenotypes should be selected for in populations species. Within vertebrate ectotherms, four dermal occupying cool and low solar radiation areas, given that cell layers influence colouration. Near the epidermis, dark colouration confers a low skin reflectance—and xanthophore and/or erythrophore pigment cells produce hence faster heat absorption—compared to lighter yellows and oranges, iridophores in the middle layer phenotypes under similar conditions (Watt, 1968; produce structural colours ranging from white to Clusella-Trullas et al., 2007). While there exists some purple, and melanophores, in the deepest dermal layer, convincing evidence for the thermoregulatory benefits produce blacks and browns (Shawkey and D’Alba, of melanism (e.g., Gibson and Falls, 1979; Clusella- 2017). Colouration is thus the product of differential Trullas et al., 2008, 2009; Muri et al., 2015), support for reflectance and absorptance of light wavelengths caused the generality of the TMH remains largely ambiguous by variation in the architecture and arrangement of these in both invertebrate (reviewed in Umbers et al., 2013) pigmentary and structural components of the dermal and vertebrate (reviewed in Geen and Johnston, 2014) system (Bechtel, 1978; Shawkey and D’Alba, 2017). ectotherms. This lack of consensus is partly because One conspicuous colour form is melanism, wherein melanism may arise through other modes of selection individuals are partially or entirely dark in appearance unrelated to (or in concert with) thermoregulation, (Majerus, 1998; True, 2003). Melanism can occur as such as crypsis, communication and protection from discrete or continuous variation within a species (i.e., as damaging amounts of ultraviolet radiation (True, 2003; a polymorphism), or as fixed colour differences between Matthews et al., 2016; Stuart-Fox et al., 2017). closely related species (reviewed in True, 2003). Within Another caveat of many previous studies is that they reptiles, melanistic phenotypes are typically produced only examine one or very few closely related species by an overabundance of melanophores (dark pigment- (e.g., Gibson and Falls, 1979; Capula and Luiselli, containing cells) or an absence of the more superficial 1994; Forsman, 1995; Janse van Rensburg et al., 2009) xanthophores and iridophores (Morrison et al., 1995; and, by virtue of their small scope, have limited ability Kuriyama et al., 2016). Furthermore, some ectotherms to address the relevance of the TMH for ectotherms are capable of ontogenetic, seasonal or rapid skin- more generally. The necessary next step in addressing darkening in response to various internal and external the TMH is to use large-scale investigations at different stimuli (reviewed in Stuart-Fox and Moussalli, 2009; levels of organisation, such as among individuals, Olsson et al., 2013). populations, and species (Clusella-Trullas et al., 2008). Studies investigating the evolutionary fitness of Of course, such investigations first require sufficient melanistic phenotypes within ectothermic species and information about the occurrence of melanism in a populations have largely centred around the ‘thermal wide variety of model systems. Further observations melanism hypothesis’ (herein TMH; reviewed in of melanistic phenotypes in wild specimens can increase our repertoire of model systems with which to investigate the processes driving the emergence and maintenance of melanism. Thus, I present a rare observation of melanism in a wild blue-tongue (genus 1 Biosis Pty Ltd, Port Melbourne, Victoria 3207, Australia. E-�� Tiliqua) from Australia—a country in which there are mail: [email protected] few documented cases of melanistic polymorphisms. © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. 252 Jules E. Farquhar

Materials and Methods all present day captive melanistic T. scincoides have descended (R. Shine, pers. comm.). This first melanistic Study species. Tiliqua scincoides (White, 1790) is a female was bred with a normally-pigmented male, and large diurnal scincid with two recognised subspecies in the resulting offspring all displayed normal pigmentation. Australia; the nominate subspecies Tiliqua s. scincoides One of the normally-pigmented (but heterozygous for (eastern blue-tongued lizard) occurs in south-eastern melanism) male progeny was bred with the original Australia, whereas Tiliqua s. intermedia Mitchell, melanistic female, producing litters with phenotypic 1955 (northern blue-tongued lizard) occurs exclusively ratios of approximately 75% normally pigmented, 25% in the tropical north. Considering only the nominate melanistic (J. Ball, pers. comm.). Hence, it appears that subspecies herein, T. scincoides is common throughout melanism in T. scincoides is a recessive trait displaying virtually all habitats in its range excluding alpine and simple Mendelian inheritance, manifesting only in rainforest environments (Cogger, 2014; Wilson and individuals that are homozygous for melanism (e.g., Swan, 2017). While colour and pattern are variable in Blanchard and Blanchard, 1941; Bechtel, 1978; King, this species, specimens typically are pale grey to brown 2003). This has now been amply confirmed through above with a series of darker brown transverse bands years of extensive breeding of melanistic T. scincoides on the body and tail (Cogger, 2014; Wilson and Swan, in captivity (J. Ball, pers. comm.). 2017; e.g., Fig. 1A). Observation. At 16:05 h on 2 November 2016, a In January 1998, the first melanistic T. scincoides, a melanistic T. scincoides was observed basking on a rock neonatal female, was found on Narrabeen Beach in New along a vegetated bank of the Barwon River in the coastal South Wales; this is the female specimen from which city of Geelong, Victoria (-38.1618°S, 144.3224°E; 5 m a.s.l.). The Barwon River provides a corridor of remnant floodplain riparian woodland habitat through the otherwise heavily modified suburbs of Geelong. Ambient temperature at the time of observation was 15.5 ºC, with 60% relative humidity (Bureau of Meteorology, www.bom.gov.au). The basking site was a series of artificially placed rocks used to delineate the edge of a short section of a walking trail, located 20 m from the river’s edge. The specimen was uniformly very black above, with the series of transverse bands across the body and tail being only scarcely discernible (Fig. 1B). The lower flanks were pale brown, being slightly lighter than the dorsum, and the ventral surface was much lighter again, being closely resemblant of the ventral colour pattern seen in normally-pigmented individuals. No physiological or ontogenetic colour change occurs in the species (Geen and Johnston, 2014), hence the specimen’s dark appearance is considered to be a fixed melanistic phenotype. The sex of the specimen was not determined.

Discussion Melanism has been reported in other Tiliqua species, including in a blotched blue-tongued lizard Tiliqua nigrolutea (Quoy and Gaimard, 1824) from Hobart, Figure 1. Photographs showing colour polymorphism in wild Tiliqua s. scincoides. (A) A normally-pigmented specimen Tasmania and in some highland populations of the from south-eastern South Australia, the typical appearance of shingleback Tiliqua rugosa (Gray, 1825) in NSW the species throughout its range. (B) the melanistic specimen (Shea, 1999). Despite the ubiquity of T. scincoides in from the Barwon River in Geelong, Victoria (photographs by south-eastern Australia, the observation presented here J. Farquhar). constitutes only the second formally documented case Melanism in the eastern blue-tongued lizard from south-eastern Australia 253 of melanism in this species, and the first in Victoria. conspecifics. This demonstrated thermal advantage of The first formally published case of melanism in T. melanism in T. scincoides, coupled with the 10 coastal scincoides (Woodall, 2000) was of a specimen from observations of melanistic specimens, indicates that Peel Island in Moreton Bay, Queensland (QLD). melanism may represent a thermal adaptation among One explanation for the apparent scarcity of records is some coastal populations of T. scincoides. that, being a recessive trait in T. scincoides (J. Ball, pers. There is also convincing inferential support from the comm.), melanism may naturally occur at low frequencies literature suggesting that melanism may constitute a in wild populations. Indeed, within polymorphic lizard coastal adaptation. Firstly, melanism has been reported populations in the northern hemisphere, the frequency in many reptile species and populations occurring near of melanism is typically low: 0.05% (San-Jose et al., or within peninsula, insular or otherwise cool coastal 2008; Kuriyama et al., 2016); 2.5% (Jambrich and habitats (e.g., Brown, 1991; Castilla, 1994; Pearse Jandzik, 2012); 8.3% (Gvozdik, 1999). and Pogson, 2000; Mashinini et al., 2008; Janse van On the other hand, it is possible that melanism in Rensburg et al., 2009; Kuriyama et al., 2016). Indeed, wild T. scincoides is more common than is currently in one of few examples of melanistic polymorphisms recognised, and the perceived rarity of this phenotype in Australia’s venomous snakes (Squamata: Elapidae), may reflect, in part, a lack of documentation. Through several island and peninsula populations of tiger personal communications and a review of all photographs snakes Notechis scutatus (Peters, 1861) are entirely of wild T. scincoides associated with georeferenced melanistic (Cogger, 2014). Second, distribution records submitted to the Atlas of Living Australia modelling of cordylid lizards (Janse van Rensburg (ALA, www.ala.org.au), I have confirmed eight et al., 2009) and a scincid lizard (Portik et al., 2010) additional observations of melanism in T. scincoides from south-western South Africa has shown that from New South Wales (NSW) and Victoria (Vic.), at melanistic species and populations are associated with the following locations: Narrabeen Beach, NSW, 1998 cool, cloudy/foggy climates in coastal areas. Finally, (R. Shine, pers. comm.); Dee Why, NSW, 2017 (M. molecular investigations show that coastal melanistic Crawford, pers. comm.); Allambie Heights, NSW, 2020 populations of the California legless lizard Anniella (ALA record); Buckley Falls, Geelong, Vic., 2012 (K. pulchra Gray, 1852 (Pearse and Pogson, 2000), Karoo Bell, pers. comm.); Belmont, Geelong, Vic., 2016 (ALA girdled lizard Karusasaurus polyzonus (Smith, 1838) record); Belmont, Geelong, Vic., 2019 (ALA record); (Engelbrecht et al., 2011), and tiger snake N. scutatus Bellbrae, Vic., 2019 (T. Sullivan, pers. comm.); Greater (Keogh et al., 2005) are genetically interdigitated with Geelong area, Vic., 2020 (ALA record). Photographs of non-melanistic conspecifics, suggesting that melanism all accounts showed extremely dark individuals which can independently emerge from a parallel evolutionary closely resemble the Geelong specimen of Figure 1B. response to selection in cold coastal environments. Together, the two formally published (Woodall, 2000; There is a possibility that some of the more recent reports this paper) and eight unpublished observations indicate of melanistic T. scincoides are simply escaped pets from three general localities where melanism occurs in wild people’s homes, given that melanistic T. scincoides have T. scincoides: the Greater Geelong area (Vic.), the become popular among private reptile keepers and are northern Sydney area (NSW); and Peel Island (QLD). readily available for purchase. Indeed, most of the recent Interestingly, all the aforementioned observations of records are within suburban environments. This could be melanistic T. scincoides are in coastal areas. Coastal resolved by comparing the genetic relatedness of wild areas are significantly cooler, wetter, foggier, and less specimens with captive specimens. For example, if the seasonal than inland areas (Janse van Rensburg et al., recent specimens observed around Geelong (Vic.) have 2009; Weigelt et al., 2013), thus selection may favour arisen independently of the northern Sydney (NSW) melanism (i.e., low skin reflectivity) to improve heat population under parallel selection for melanism, we absorption under these conditions of low solar radiation would expect them to be related to wild normally- and low ambient temperatures; the core prediction pigmented specimens occurring in the same area. of the TMH (Clusella Trullas et al., 2007, 2008). In However, if melanistic Geelong specimens are instead concordance with this prediction, Geen and Johnston more closely related to captive melanistic specimens, (2014) have demonstrated that captive melanistic and hence the Sydney locality from which all captive T. scincoides have lower skin reflectivity, which specimens are derived, we could conclude that they are enables faster heat gain compared to non-melanistic escaped pets. 254 Jules E. Farquhar

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Accepted by Saeed Hosseinian Yousefkhani