Evolution, Conservation and Cane Toads in Australia
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1 INTRODUCTION EVOLUTION, CONSERVATION AND CANE TOADS IN AUSTRALIA 2 CONTEMPORARY EVOLUTION IN CONSERVATION There is an increasing realisation amongst biologists that evolution can occur rapidly – on time scales generally associated with “ecological time” (Stockwell et al. 2003; Thompson 1998). It is interesting that biologists have only recently incorporated the concept of “contemporary evolution” into their worldview. We have known since before the modern synthesis that, per generation, the response to selection (R) in a trait is equal to the heritability of that trait (h2) multiplied by the strength of selection (S) operating in that generation (Lynch and Walsh 1998): R = h 2S This apparently simple equation tells us much about the nature of adaptation, not the least of which is that it can happen rapidly; dependent upon high heritability and strong selection acting within the range of variability for the trait in question. We have also had, for many years, empirical evidence that under the right conditions evolution precedes rapidly from strong selection in natural populations (e.g. Kettlewell 1973). Why then, has it taken so long to appreciate the potential importance of evolution acting along timescales that are of relevance to our everyday existence? This is a question for a science historian – which I am not – but perhaps one of Gould’s (1991) creeping fox-terrier clones is to blame: Someone (perhaps Darwin himself, who as it turns out, was occasionally confused about the difference between microevolution and 3 speciation), told us that evolution takes a long time, and we have been repeating this mantra to ourselves and our students ever since. Nevertheless, contemporary evolution has slapped us in the face until we have had no choice but to pay it some attention. Predictably in hindsight, contemporary evolution first became apparent in areas of our lives that we care deeply about; our health and our food. The green revolution and its attendant barrage of pesticides was, on reflection, a thoroughly unintended experiment in evolution. Pesticides, that were initially incredibly effective became increasingly less so as pests rapidly evolved resistance (Palumbi 2002). Similarly, the discovery of antibiotics seemed set to save us from the scourge of disease (well, most of them anyway). Over time, our magic bullets have often come to resemble peashooters; many pathogens evolving either flak jackets or the simple ability to dodge (Ewald 1994). Two of the biggest human- killers on the planet – malaria and HIV – have achieved this position of prestige precisely because of their ability to evolve at such speed that our attacks continually hit nothing but air (Gardner et al. 2002; Palumbi 2002). We have no choice but to acknowledge evolution when it foils our plans, but we often fail to appreciate that it can also be useful. Domestication is, of course, evolution by human selection (blessed are the pigeon fanciers, for they shall convince Darwin of the truth). And recently, medical and agricultural researchers are realising that evolutionary problems require evolutionary solutions – “evolutionarily stable strategies” are the new weapons in the wars 4 against Malaria, HIV and pesticide resistance (Ewald 1994; Palumbi 2002; Rausher 2001). But let us step aside from directly human-oriented concerns and apply a worldview of contemporary evolution to conservation. There is little doubt that we are living in a time of accelerated extinction (Chapin et al. 2000; May et al. 1995). Species are going extinct at higher than normal rates due to the activities of our species. Like all species, we interact with the world and, as a consequence, modify it. Unlike most species however, our modifications are large and global in their reach. In the dry language of science however, our impacts are nothing more than “environmental change”, and a geological perspective tells us that environmental change is not a new phenomenon; continents have moved, climate has changed, land bridges have allowed mass invasions, and mountains have come and gone (Morrison and Morrison 1991). Ultimately, species either evolve through environmental change or they go extinct: Even Raup’s (1993) extinction through bad luck will almost always be the result of an environmental change. The activities of humans are causing rapid, global environmental modifications; the rapidity and size of these changes are causing an increase in the extinction rate. Understanding how to reduce or reverse the effect of human-mediated impacts on species and communities has become the province of conservation biology. Conservation biologists know that they are fighting an uphill battle and are well aware that the resources do not come close to matching the extent of the problem. Strategies and priorities thus need to be effective and as 5 efficient as possible. It is in this desperate, outnumbered rearguard that contemporary evolution is a mostly ignored, but potentially powerful ally. It is a property of living systems that they evolve – they are inherently dynamic and we know that evolution can happen in ecological time. Evolutionary time is, like all time, relative; in the case of evolution, time is relative to the generation time of the organism. If an environmental change occurs along a time scale that is not too rapid, a population can mount an adaptive response. In other words, if the per generation strength of selection (S) is not too large there is a good chance of evolution instead of extinction. Evolved adaptation is (almost by definition) the best “strategy” for the long- term persistence of a species; from a conservation perspective, whether or not a species will adapt to a change is more important than whether it suffers short- term impact. For conservationists, overwhelmed by the sheer number of species potentially at risk from human activities, the contemporary evolution perspective suggests that the problem may be slightly smaller than it otherwise looks. An ability to evolve around environmental change may see many species rescue themselves. The challenge for conservation biologists is to understand which species are likely to exhibit rapid evolution and which categories of environmental change are likely to encourage evolution rather than extinction. Organisms with short generation times relative to the pace of change will have evolution on their side. Similarly, environmental changes that are 6 relatively slow and cause selection on traits that are unlikely to have been previously important for fitness will encourage evolution. Conservation biologists need to start understanding where the boundaries lie in these continuums: When does an environmental change become too rapid to expect an evolved response from an impacted species? When does the generation time of an organism become too long to preclude adaptive response to an instantaneous change of a given magnitude? These kinds of questions are not necessarily simple to answer but in answering them we can have a profound impact on the size of the conservation battle. Perhaps less species are in need of “rescuing” than we currently believe and perhaps some environmental changes are less important than others. This thesis represents an attempt at a small piece of this puzzle. In the pages that follow, I examine the potential for Australian snake species (which have relatively long generation times of 1-3 years) to adapt to a strong and instantaneous shift in their selective environment; the invasion of a toxic prey item. 7 SNAKES AND TOADS IN AUSTRALIA “To others who scent a ‘nigger in the woodpile’ and suggest the possibility that the toad will, in turn, itself become a pest, we can point to the fact that nearly 100 years have elapsed since it was first introduced into Barbados, and there it has no black marks against its character. Experience with it in other West Indian islands and in Hawaii, certainly points to the fact that no serious harm is likely to eventuate through its introduction into Queensland” R W Mungomery upon returning to Australia from Hawaii with 101 toads in 1935. Australia has a particularly diverse reptile fauna, among which we count around 140 native, terrestrial snake species (Cogger 2000). Thirty-three of these species are typhlopids – mostly blind, burrowing eaters of ant and termite eggs. The remaining terrestrial species belong to the colubrid, pythonid and elapid families and eat vertebrate prey. Of these, the colubrids (11 species) are relatively recent colonisers of the continent, probably arriving from south-east Asia during the glaciations of the early Pleistocene (2 mya, Greer 1997). The pythons (15 species) and elapids (81 species) have been present much longer, at least since the early Miocene (ca. 20 mya, Shine 1991a). Australia’s snakes (even the newer ones!) have a long history on the Australian continent. This venerable history contrasts garishly against the history of Bufo marinus. The species was variously referred to as the “giant toad” or “marine toad” by authors of the early part of this century (e.g. 8 Kinghorn 1938), however it is now known through most of its introduced, English-speaking range as the “cane toad” (Lever 2001) – a fitting epithet for a species that has benefited so profoundly from the sugar-cane industry. Originally from South America, the global sugar industry, in a welter of small, poorly thought out decisions, introduced cane toads throughout much of the Caribbean and Pacific (Easteal 1981). It was the sugar industry that brought toads to Australia in 1935; in simple wooden crates, 101 toads were shipped from Hawaii to Gordonvale in north Queensland where, it was hoped, they were to save the sugar farmers from crop-ruining beetle pests (Mungomery 1935). The plan was that the toads were to eat their way through the cane beetle populations, leaving farmers with little beetle-filled faeces and healthy crops. The plan wasn’t a notable success and by the 1940s toads were made entirely redundant by the development of pesticides (Low 1999).