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Four Darwinian Themes on the Origin, Evolution and Preservation of Island Journal of Biogeography (J. Biogeogr.) (2010) 37, 985–994 SPECIAL Four Darwinian themes on the origin, ISSUE evolution and preservation of island life Mark V. Lomolino* College of Environmental Science and Forestry, ABSTRACT Syracuse, NY 13210, USA Charles Darwin’s observations and insights continue to inspire nearly all scientists who are captivated by both the marvels and the perils of island life. Here I feature four themes inspired by Darwin’s singular insights: themes that may continue to provide valuable lessons for understanding the ecological and evolutionary development of insular biotas, and for conserving the natural character and evolutionary potential of all species restricted to isolated ecosystems (natural or anthropogenic). *Correspondence: Mark V. Lomolino, College of Keywords Environmental Science and Forestry, Syracuse, NY 13210, USA. Assembly, biogeography, Charles Darwin, conservation, evolution, extinction, E-mail: [email protected] islands. ‘As with shipwrecked mariners near a coast, it would have been on the decline of nature over a century before ‘biodiversity’ better for the good swimmers if they had been able to swim still and ‘conservation biology’ were first articulated. further,…’ Here I provide an historical and prospective overview of the ‘A gun is here almost superfluous...’ development of theory on the ecological and evolutionary ‘It is impossible to reflect on the changed state of the American assembly of insular biotas and, in particular, the continuing continent without the deepest astonishment.’ capacity of island studies to provide fundamental insights for ‘Humboldt saw in South America a parrot which was the sole living conserving the diversity and natural character of native biotas. creature that could speak a word of the language of a lost tribe…’ In forming his theory of natural selection, Darwin drew heavily on studies of the effects of artificial selection on domestic livestock. Thus, I see fitting irony and symmetry in the INTRODUCTION prospect that the tables should now be turned; that our The above excerpts of quotations from Charles Darwin’s abilities to predict and hopefully mitigate the effects of writings, which I present and discuss in detail below, capture artificial selection incurred through species introductions, themes that proved seminal for generations of scientists who overharvesting and anthropogenic insularization (via habitat were equally captivated by both the marvels and the perils of loss and fragmentation) rest heavily on the revelations of island life. Although presented as I have done so above as Darwin and generations of countless others who studied the disarticulated and seemingly unrelated metaphors and observa- effects of natural selection on isolated biotas. The relevance of tions, these passages from Darwin’s publications serve as mile island studies is only likely to increase as their native biotas markers along a professional and personal journey shared by become ever rarer, and as an increasing proportion of most scientists who study island life: one that progresses from an continental biotas become more restricted to island-like innate attraction for insular biotas, to an astonishment over their ecosystems (e.g. wildlife parks, nature reserves and other rem- distinct and seemingly bizarre character, a quest to explain these nants of once expansive and continuous, native ecosystems). phenomena in the most fundamental terms, and finally to a My purpose here is to discuss four themes inspired by the sobering understanding of the fragility of island life and of our research and writings of Charles Darwin; themes on the obligations as scientists and the planet’s only global stewards to assembly (and disassembly) of insular biotas which continue to conserve these imperilled biotas. hold great promise for providing insights into their ecological Darwin, of course, was not the first naturalist to study the and evolutionary development, and for conserving the natural diversity and singular nature of island life, but his classic works character and evolutionary potential of species restricted to clearly constitute a seminal nexus in the reticulating phylogeny isolated ecosystems (natural or anthropogenic). The first of island theory. Perhaps just as important, Darwin remarked theme describes how selective pressures on islands are often ª 2009 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi 985 doi:10.1111/j.1365-2699.2009.02247.x M. V. Lomolino reversed from those in species-rich, taxonomically balanced ‘As Professor Owens has remarked, there is no greater anomaly in communities of the continents. The second and third themes nature than a bird that cannot fly.’ address resultant effects of those reversals in selection forces, (Darwin, 1859, pp. 175–176) ¨ ´ including the development of naıvete and the fragility of The anomaly, however, was rendered explicable by Darwin’s insular biotas, and the downsizing (through megafaunal eloquent metaphor of shipwrecked mariners. The natural extinctions) and evolutionary convergence on phenotypes that ontogeny of island endemics is one of regular and highly are optimal in species-poor and disharmonic communities of predictable reversals in natural selection from that for the ‘good remote, oceanic islands. The final theme addresses the swimmers’ during immigration, to selection for those adapted to geography of extinction which, seemingly paradoxically to the special nature of insular environments following coloniza- the general fragility of insular biotas, is characterized by tion. Many hundreds of birds, insects and plants – in succumb- persistence of the most isolated populations. ing to the pressures for ‘sticking to the wreck’ – ultimately lost Most examples and case studies that I discuss here are of the capacity to disperse to other islands (see McNab, 1994). terrestrial systems, especially vertebrates. I leave it to others to explore the heuristic and applied relevance of these themes to other ecosystems and taxa. Theme 2. The perils of splendid isolation ‘A gun is here almost superfluous; for with the muzzle I pushed a hawk off the branch of a tree.’ FOUR DARWINIAN THEMES ON THE ASSEMBLY (Darwin, 1860, Ch. 17, Galapagos Archipelago) OF INSULAR BIOTAS Reversals in natural selection are at the heart of explanations Theme 1. Reversals in natural selection: from for not only the many marvels of island life, but its fragility as ‘swimming’ to ‘sticking to the wreck’ well. That is, selection for adaptation to the special nature of ‘As with shipwrecked mariners near a coast, it would have been insular environments – which include not just their isolation better for the good swimmers if they had been able to swim still and limited area, but the depauperate and disharmonic nature further, whereas it would have been better for the bad swimmers if of their communities – results in fundamental transformations they had not been able to swim at all and had stuck to the wreck.’ in the character of insular species. In addition to the striking (Darwin, 1859, p. 177) anomalies of flightless birds and insects discussed by Darwin I begin with the above passage from The Origin because it and many others, these transformations include a suite of provides a conceptual framework fundamental to understand- equally remarkable reversals in morphology, physiology and ing the ecological and evolutionary assembly of island life: behaviour in countless other species – ecological and evolu- reversals in selective pressures which produce both the marvels tionary adaptations of insular species to remote island and perils of island life. Darwin used the first part of this communities, which are typically free of terrestrial mammals. metaphor to explain a type of natural selection quite different Under these conditions, both plants and animals often lose the from ‘survival of the fittest’. That is, he envisioned this form of structures and behaviours essential for predator (carnivore and natural selection occurring during immigration to very isolated herbivore) avoidance on the mainland (Carlquist, 1965, 1974; islands, and resulting in founding populations biased in favour Lomolino et al., 2006; Whittaker & Ferna´ndez-Palacios, 2007). of individuals with superior immigration abilities. Unlike drift On the mainland, interspecific interactions in species-rich and random founding effects, immigrant selection (sometimes and ecologically balanced communities can drive ecological termed ‘selection for thrifty genotypes’ by anthropologists; and evolutionary divergence among species; some plants Neel, 1962) can explain directional trends in the structure of avoiding competition and herbivory by dispersing to colonize insular communities and populations (e.g. towards dishar- ephemeral habitats and growing and reproducing rapidly (as mony and dominance of particular, highly vagile species or herbaceous forms), others investing more in arsenals of thorns phenotypes: see Darlington, 1957; Carlquist, 1966a,b; Lomo- and defensive chemicals. In animals, divergence in body size on lino, 1984, 1993; and Bindon & Baker, 1997). the continents may be in response to selective pressures to Of even more fundamental importance in terms of under- reduced competition or escape predators; e.g. some species standing the special nature of insular biotas is the second part decreasing in size and thus becoming more capable of finding of Darwin’s metaphor because it cogently asserts that selective shelter in burrows or under rocks and logs; others increasing in pressures vary – but
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