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TRENDS in Ecology and Evolution Vol.23 No.1
Letters Response
Response to Köhler 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, Ancón, Panamá, República de Panamá
I welcome the response of Köhler et al. [1] to my recent
article [2], in which I discussed the controversy surrounding the interpretation of Homo floresiensis, a fossil hominin
from the island of Flores [3]. Köhler 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.
floresiensis.
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’
Köhler 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. floresiensis 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 specifically to H. floresiensis 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 Köhler et al. that
’Island rules cannot be broken’ is simply not justified. Interestingly, primates do conform to this original island rule and
the amount of reduction of body mass in H. floresiensis
(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 specific 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. [email protected], [email protected].
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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
beneficial for the survival of an island mammal.
Köhler and colleagues mention two specific aspects of H.
floresiensis morphology that they claim violate island rules
– sense organ and brain size and limb morphology. Yet for
the reasons just discussed, we cannot predict specific
changes in brain volume and sense organs or in limb
morphology after isolation on an island, because this will
depend upon the specific 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 efficiency, 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.
floresiensis with those of apes, humans and other fossils
suggests that it retains a primitive morphology [11].
In short, Köhler and colleagues suggest that current
knowledge of mammalian evolution on islands is sufficiently complete that we can exclude the existence of
species falling outside our expectations. Because we cannot
define 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]).
Köhler and colleagues deem H. floresiensis 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. floresiensis 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 Köhler, M. et al. (2008) Island rules cannot be broken. Trends Ecol. Evol.
23, 6–7
Update
2 Niven, J.E. (2007) Brains, islands and evolution: breaking all the rules.
Trends Ecol. Evol. 22, 57–59
3 Brown, P. et al. (2004) A new small-bodied hominin from the Late
Pleistocene of Flores, Indonesia. Nature 431, 1055–1061
4 Foster, J.B. (1964) Evolution of mammals on islands. Nature 202, 234–
235
5 Damuth, J. (1993) Cope’s rule, the island rule and the scaling of
mammalian population density. Nature 365, 748–750
6 Bromham, L. and Cardillo, M. (2007) Primates follow the island rule:
implications for interpreting Homo floresiensis. Biol. Lett. 3, 398–400
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. 57–78, 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. Écol.
(Terre Vie) 62, 105–168
TRENDS in Ecology and Evolution Vol.23 No.1
9 Fukami, T. et al. (2007) Immigration history controls diversification in
experimental adaptive radiation. Nature 446, 436–439
10 Niven, J.E. et al. (2007) Fly photoreceptors demonstrate energyinformation trade-offs in neural coding. PLoS Biol. 5, 828–840
11 Tocheri, M.W. et al. (2007) The primitive wrist of Homo floresiensis and
its implications for hominin evolution. Science 317, 1743–1745
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 flies (Diptera: epsidae), and the
question of developmental constraints. Evol. Dev. 3, 206–222
14 Spoor, F. et al. (2007) Implications of new early Homo fossils from
Ileret, east of Lake Turkana, Kenya. Nature 448, 688–691
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 fill 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 volume’s
title – Biogeography in a Changing World – might suggest
Corresponding author: Lomolino, M.V. ([email protected]).
mistakenly to some a focus on climate change and recent,
anthropogenic modifications 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 definitions of biogeography and then briefly summarize the history of the field, 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 field 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, scientific 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 scientific and not personal grounds.
The first 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
Parenti’s chapter is the first in this volume to review and
critique the current state of the field 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 Grehan’s chapter is a more specialized one,
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