Update

Letters Response

TRENDS in Ecology and Evolution Vol.23 No.1

Response to Kohler et al.: Impossible arguments about possible species?

Jeremy E. Niven1,2
1 2

Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancon, Panama, Republica de Panama

I welcome the response of Kohler et al. [1] to my recent article [2], in which I discussed the controversy surrounding the interpretation of Homo oresiensis, a fossil hominin from the island of Flores [3]. Kohler and colleagues present alternative arguments and interpretations of the evidence. However, these arguments rely on assumptions that under close scrutiny do not justify revising the status of H. oresiensis. The island rule describes the tendency of larger-bodied species to become dwarfed whereas small-bodied species become enlarged relative to their mainland counterparts when they are isolated on islands [4,5]. To this original rule Kohler et al. add changes in additional factors, including energy metabolism, brain size and sense organs [1]. Several of the factors (e.g. reduction of expensive locomotor behaviours, enhanced fat storage, increased lifespan) that they incorporate into the island rule are based on observations from a few species and, therefore, do not constitute a demonstration of a general trend among all mammals on islands. They state that because H. oresiensis does not conform to their new set of island rules, it cannot be a valid species. I have several objections to this argument whether applied specically to H. oresiensis or more generally. The original island rule is supported by empirical evidence [4,5] but it remains a correlation in which there is considerable variability among species and numerous exceptions both at the level of single species and entire mammalian orders. The declaration of Kohler et al. that Island rules cannot be broken is simply not justied. Interestingly, primates do conform to this original island rule and the amount of reduction of body mass in H. oresiensis (assuming either H. sapiens or H. erectus as the ancestral species) is consistent with the reduction in body mass observed in other primates isolated on islands [6]. The island rule pertains to changes in body mass and makes no specic predictions about which particular tissues should be affected [4,5]. Thus changes in body mass could be achieved in many different ways, the amounts of different expensive tissues such as brain, gut and kidney being traded-off against one another [7]. Indeed, the precise phenotypic changes that occur after isolation on an island would be expected to depend on the morphology, physiology and behaviour of that species, the size and geographical position of the island [8], and various historical processes including founder effects and the precise order in which other species colonized the island [9]. All of
DOI of original article: 10.1016/j.tree.2007.10.002. Corresponding author: Niven, J.E. jen22@cam.ac.uk, nivenj@si.edu.

these factors will affect resource availability, predation risk and competition on an island. The changes in traits resulting from these selection pressures will be expected to be benecial for the survival of an island mammal. Kohler and colleagues mention two specic aspects of H. oresiensis morphology that they claim violate island rules sense organ and brain size and limb morphology. Yet for the reasons just discussed, we cannot predict specic changes in brain volume and sense organs or in limb morphology after isolation on an island, because this will depend upon the specic selective pressures involved. This is a particularly acute problem when considering brain evolution, because we are only just beginning to understand the relationships between energy consumption, energy efciency, neural processing and body mass [10]. Yet this is also a problem when considering limb morphology, especially when no behavioural evidence for the locomotory gait exists. Detailed comparative analysis and modelling are essential before inferences can be made about whether limb morphology could support particular gaits. Indeed, a recent comparison of the wrist of H. oresiensis with those of apes, humans and other fossils suggests that it retains a primitive morphology [11]. In short, Kohler and colleagues suggest that current knowledge of mammalian evolution on islands is sufciently complete that we can exclude the existence of species falling outside our expectations. Because we cannot dene the limits of evolutionary possibility, we cannot consign a species to being impossible. Some possibilities might seem remote (for discussion see Ref. [12]) but nevertheless lineages sometimes evolve remarkable innovations under certain circumstances (for example, see Ref. [13]). Kohler and colleagues deem H. oresiensis an impossible species by assuming constraints on evolutionary possibility for which they have little evidence. Thus, as I stated in my original article, it seems too early to dismiss the claim that H. oresiensis is a new hominin species. Indeed, recent fossil evidence suggests that there might have been considerably more variability in hominin body size than previously appreciated [14], emphasizing the need to keep an open mind.
Acknowledgements
I thank Bill Eberhard and Mary Jane West-Eberhard for helpful comments.

References
1 Kohler, M. et al. (2008) Island rules cannot be broken. Trends Ecol. Evol. 23, 67

Update
2 Niven, J.E. (2007) Brains, islands and evolution: breaking all the rules. Trends Ecol. Evol. 22, 5759 3 Brown, P. et al. (2004) A new small-bodied hominin from the Late Pleistocene of Flores, Indonesia. Nature 431, 10551061 4 Foster, J.B. (1964) Evolution of mammals on islands. Nature 202, 234 235 5 Damuth, J. (1993) Copes rule, the island rule and the scaling of mammalian population density. Nature 365, 748750 6 Bromham, L. and Cardillo, M. (2007) Primates follow the island rule: implications for interpreting Homo oresiensis. Biol. Lett. 3, 398400 7 Aiello, L.C. et al. (2001) In defense of the expensive tissue hypothesis. In Evolutionary Anatomy of the Primate Cerebral Cortex (Falk, D. and Gibson, K.R., eds), pp. 5778, Cambridge University Press 8 Leigh, E.G. et al. (2007) The biogeography of large islands, or how does the size of the ecological theatre affect the evolutionary play? Rev. Ecol. (Terre Vie) 62, 105168

TRENDS in Ecology and Evolution Vol.23 No.1

9 Fukami, T. et al. (2007) Immigration history controls diversication in experimental adaptive radiation. Nature 446, 436439 10 Niven, J.E. et al. (2007) Fly photoreceptors demonstrate energyinformation trade-offs in neural coding. PLoS Biol. 5, 828840 11 Tocheri, M.W. et al. (2007) The primitive wrist of Homo oresiensis and its implications for hominin evolution. Science 317, 17431745 12 Authur, W. (2004) Biased Embryos and Evolution. Cambridge University Press 13 Eberhard, W.G. (2001) Multiple origins of a major novelty: moveable abdominal lobes in male sepsid ies (Diptera: epsidae), and the question of developmental constraints. Evol. Dev. 3, 206222 14 Spoor, F. et al. (2007) Implications of new early Homo fossils from Ileret, east of Lake Turkana, Kenya. Nature 448, 688691
0169-5347/$ see front matter. Published by Elsevier Ltd. doi:10.1016/j.tree.2007.10.004

Book Review

Biogeography emerging: provocative and integrative perspectives in historical biogeography

Biogeography in a Changing World by Malte C. Ebach and Raymond S. Tangney, CRC Press, 2007. US$89.95, hbk (212 pages) ISBN 978 0 8493 8038 9

Mark V. Lomolino
Department of Environmental and Forest Biology, SUNY College of Environmental Science and Forestry, Syracuse, NY 13210, USA

Well, perhaps you can judge a book by its cover, at least to some extent. Artist Neal Adams was commissioned by the editors of this collected volume of essays to illustrate a still far from mainstream, yet captivating, theory on the dynamics of the earth the expanding earth theory championed by a select group of individuals (most notably S. Warren Carey) from the 1950s to 1980s. The theory remains an unaccepted, but perhaps unappreciated, explanation for the dynamics of the continents and their respective biotas, which drifted apart as a small, primordial, continental earth expanded and ocean basins developed to ll in the gaps. The cover illustration, thus, serves as a captivating declaration that this collection of essays will be, if nothing else, provocative and will challenge traditional views of how regional biotas develop over time. The book is the product of a symposium entitled What is Biogeography?, which took place during the Fifth Biennial Meeting of the Systematics Association in 2005. The stated goal of the symposium was to present a broad-based perspective on the nature of biogeography, offering historical perspectives based on current understanding and methodological advances, as well as what the future might hold. One underlying theme for several essays in this volume is that geographic variation among biotas is not only shaped by geological dynamics but also that these biogeographical patterns can inform and, at times, challenge our current understanding in geology. Thus, although the volumes title Biogeography in a Changing World might suggest
Corresponding author: Lomolino, M.V. (island@esf.edu).

mistakenly to some a focus on climate change and recent, anthropogenic modications in landscapes and their dependent biotas, it seems entirely appropriate within the context of historical development of the earth and its biotas. In their introduction to this volume, the editors discuss various denitions of biogeography and then briey summarize the history of the eld, focusing on different approaches for reconstructing the historical development of regional biotas. As almost every student of historical biogeography realizes quickly, the history of this eld is fraught with contentious debates among alternate schools, which often degrade into contemptuous clashes among their champions. Although controversy is of course part and parcel of most, if not all, scientic crisis and revolutions [1], a rapprochement among debating schools and a reintegration of long divergent lines of study will be best served if these debates are tempered and waged on scientic and not personal grounds. The rst chapter, by David M. Williams, chronicles one of these legendary clashes the debates between Ernst Haeckel and Louis Agassiz and their students over the utility of the threefold parallelism (the synthesis of paleontology, systematics and ontogeny) and the importance of geographic variation in reconstructing genealogies. Lynne Parentis chapter is the rst in this volume to review and critique the current state of the eld and to discuss potential synthesis among its various camps, in particular, cladistic and phylogenetic biogeography. Here, she presents a cogent and persuasive argument for achieving a new synthesis, which Donn Rosen called for nearly three decades ago: a revolution in the earth sciences an integrated natural history of the geological and biological systems. John Grehans chapter is a more specialized one,
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