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Rapid and Repeated Origin of Insular Gigantism and Dwarfism in Australian Tiger Snakes

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Rapid and Repeated Origin of Insular Gigantism and Dwarfism in Australian Tiger Snakes Evolution, 59(1), 2005, pp. 226±233 RAPID AND REPEATED ORIGIN OF INSULAR GIGANTISM AND DWARFISM IN AUSTRALIAN TIGER SNAKES J. SCOTT KEOGH,1 IAN A. W. SCOTT, AND CHRISTINE HAYES School of Botany and Zoology, The Australian National University, Canberra, ACT, 0200, Australia 1E-mail: [email protected] Abstract. It is a well-known phenomenon that islands can support populations of gigantic or dwarf forms of mainland conspeci®cs, but the variety of explanatory hypotheses for this phenomenon have been dif®cult to disentangle. The highly venomous Australian tiger snakes (genus Notechis) represent a well-known and extreme example of insular body size variation. They are of special interest because there are multiple populations of dwarfs and giants and the age of the islands and thus the age of the tiger snake populations are known from detailed sea level studies. Most are 5000±7000 years old and all are less than 10,000 years old. Here we discriminate between two competing hypotheses with a molecular phylogeography dataset comprising approximately 4800 bp of mtDNA and demonstrate that pop- ulations of island dwarfs and giants have evolved ®ve times independently. In each case the closest relatives of the giant or dwarf populations are mainland tiger snakes, and in four of the ®ve cases, the closest relatives are also the most geographically proximate mainland tiger snakes. Moreover, these body size shifts have evolved extremely rapidly and this is re¯ected in the genetic divergence between island body size variants and mainland snakes. Within south eastern Australia, where populations of island giants, populations of island dwarfs, and mainland tiger snakes all occur, the maximum genetic divergence is only 0.38%. Dwarf tiger snakes are restricted to prey items that are much smaller than the prey items of mainland tiger snakes and giant tiger snakes are restricted to seasonally available prey items that are up three times larger than the prey items of mainland tiger snakes. We support the hypotheses that these body size shifts are due to strong selection imposed by the size of available prey items, rather than shared evolutionary history, and our results are consistent with the notion that adaptive plasticity also has played an important role in body size shifts. We suggest that plasticity displayed early on in the occupation of these new islands provided the ¯exibility necessary as the island's available prey items became more depauperate, but once the size range of available prey items was reduced, strong natural selection followed by genetic assimilation worked to optimize snake body size. The rate of body size divergence in haldanes is similar for dwarfs (hg 5 0.0010) and giants (hg 5 0.0020± 0.0025) and is in line with other studies of rapid evolution. Our data provide strong evidence for rapid and repeated morphological divergence in the wild due to similar selective pressures acting in different directions. Key words. Genetic assimilation, haldanes, mitochondrial DNA, Notechis, phenotypic plasticity, phylogeography, rapid evolution. Received May 17, 2004. Accepted November 1, 2004. Island biota have received intense research attention from et al. 1997) and other (Madsen and Shine 1992) species. Head evolutionary biologists because they are thought to represent size of island populations of European adders appears to be less complex systems due to fewer, simpler, or stronger se- determined by the size of available prey items (Forsman lective pressures (Whittaker 1998; Schluter 2001). Body size 1991), whereas relaxation of predation pressure as opposed is the characteristic that tends to change most readily on to simple retention of an ancestral condition (phylogenetic islands, and it is a well-known phenomenon that islands can constraint) seems to have selected for large size in chuck- support populations of gigantic or dwarf forms that are sim- wallas lizards (Petren and Case 1997). A recent thorough ilar to their mainland conspeci®cs in most aspects except review of body size shifts in island populations of snakes adult body size (Case 1978). However, the variety of ex- concluded that the different sizes of prey items available on planatory hypotheses have been dif®cult to disentangle. islands was the most important determining factor in adult The most common explanations for shifts in island body snake body size (Boback 2003) size are the relaxation of predation or competition pressures Tiger snakes range across southern Australia from southern and random genetic drift, but the evolution of body size in Western Australia east to Esperance, to southern South Aus- general and body size shifts speci®cally is a complex and tralia, Victoria, Tasmania, and up the eastern coastal areas controversial issue because there are a number of other non- north of Brisbane. Tiger snakes also are found on many off- mutually exclusive explanations for the patterns we see in shore islands that are 1±30 km off the mainland in Western nature (Case 1978; Barton 1996; Whittaker 1998; Schluter Australia, South Australia, and in the Bass Strait off Tas- 2001). For example, careful ®eld experiments with the well- mania (Fig. 1). Others have quanti®ed body size variation in known Anolis lizard radiation have demonstrated that mor- island and mainland tiger snakes in detail. Based on the mea- phological shifts can occur extremely rapidly (Losos et al. surement of 860 tiger snakes by Shine (1987) and 2668 tiger 1997) and repeatedly (Losos et al. 1998) as the lizards adapt snakes by Schwaner and Sarre (1990), we know that mainland to new environments with the help of phenotypically plastic adult body size shows some regional variation but is none- traits (Losos et al. 2000). In marine iguanas the differing theless comparatively homogeneous relative to the island food energy levels available on different islands are important populations that display body size shifts. Adult mainland in determining adult body size (Wikelski and Trillmich tiger snakes typically reach sizes of approximately 78±92 cm 1997), but sexual selection in the form of sexual size di- snout-vent length (SVL) (Shine 1987; Schwaner and Sarre morphism also is involved in complex ways in this (Wikelski 1990). Some offshore islands also are populated by tiger 226 q 2005 The Society for the Study of Evolution. All rights reserved. BRIEF COMMUNICATIONS 227 FIG. 1. Distribution map of Australian tiger snakes with sample localities and body size variants noted. The insert is a blow up of the Sir Joseph Banks Group and the Port Lincoln Island Group in South Australia where islands with dwarfs (Roxby), giants (Hopkins and Williams), or typical mainland sized tiger snakes (other islands) are found within 30 kilometres of each other. snakes that reach a similar average adult size to those on the Shine 1987; Schwaner and Sarre 1988, 1990). (2) Most stud- mainland, but other islands are home to populations that ex- ies of insular body size variation have focused on a single hibit extreme shifts in adult body size relative to their main- shift in adult body size and on single islands, but in tiger land counterparts. Roxby Island is populated only by dwarfs snakes there are separate island populations of giants and that reach an average of approximately 70 cm SVL and weigh dwarfs and replicate examples of each (Schwaner 1985; less than 200 g whereas Mount Chappell Island is populated Schwaner and Sarre 1988, 1990). (3) There are many islands by giants that reach an average of approximately 120 cm but populated by tiger snakes that reach the same adult size as can range up to 160 cm SVL and well over 1 kg (Schwaner those on the mainland, including islands in the same geo- 1985; Shine 1987; Schwaner and Sarre 1988, 1990). Giant graphic area as islands populated with giants or dwarfs, im- tiger snakes of a similar size also are found on the islands plying that there have been different selection pressures act- of the Nuyts Archipelago in the Great Australian Bite and ing on the island populations that display body size shifts on Hopkins and Williams Island in the Port Lincoln and (Schwaner 1985; Shine 1987; Schwaner and Sarre 1988, Neptune Island groups in South Australia (Schwaner 1985; 1990). (4) Importantly, we also know the age of the islands Robinson et al. 1996). With the exception of one highly iso- and thus the age of the tiger snake populations from detailed lated population of dwarfs in the Flinders Ranges of South sea level studies; most are 5000±7000 years old and all are Australia, all mainland tiger snake populations that have been less than 10,000 years old (Robinson et al. 1996). examined are intermediate in adult body size to the island A number of hypotheses have been suggested to explain populations that display extreme body size shifts. body size shifts in island tiger snakes. Natural selection acting There are several key attributes of this system that make to optimize snake body size to available prey size is supported it ideal for testing alternative hypotheses: (1) In most ex- strongly by the compelling correlation between snake size amples of insular body size variation, the body size differ- and available prey size (Schwaner 1985; Shine 1987; Schwa- ences are comparatively small, but in tiger snakes the body ner and Sarre 1988, 1990), but other possibilities exist. Island size shifts are substantial and in particular the difference in tiger snakes display no obvious male-male competition and size between dwarfs and giants is extreme (Schwaner 1985; they are the top predator on all the islands on which they 228 BRIEF COMMUNICATIONS occur, and so competition, predation, and sexual selection position 71, 59-AATAGGAGGTTTAAGACCAAGACC; Elp already have been rejected as possible explanations (Schwa- 12SII, position 287, 59-GGTCGCTGGCACGAGATTGACCG ner 1985; Schwaner and Sarre 1988, 1990).
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