Dualism and conflicts in
understanding speciation
Menno Schilthuizen
Summary
Speciation is a central but elusive issue in evolutionary
biology. Over the past sixty years, the subject has been
studied within a framework conceived by Ernst Mayr and
Theodosius Dobzhansky and subsequently developed
further by numerous other workers. In this ``isolation''
theory, the evolution of reproductive isolation is a key
element of speciation; natural selection is given only
secondary importance while gene flow is considered
prohibitive to the process. In this paper, I argue that
certain elements in this approach have produced confu-
sion and irreconcilability among students of speciation.
The more prominent debates in speciation (i.e., the
species definition, sympatry/allopatry, and the role of
reinforcement) all derive from an inherent conflict
between the ``isolation'' theory and Darwin's ``selection''
view on species and speciation (in which disruptive
selection is crucial). New data, mainly from field ecology,
molecular population genetics, laboratory studies with
Drosophila
and computer analysis, all suggest that the
isolation theory may no longer be the most desirable
vantage point from which to explore speciation. Instead,
environmental selection in large populations, often
unimpeded by ongoing gene flow, appears to be the
decisive element. The traditional preoccupation with
reproductive isolation has created gaps in our knowledge
of several crucial issues, mainly regarding the role of
environmental selection and its connection with mate
selection. BioEssays 22:1134±1141, 2000.
ß 2000 John Wiley & Sons, Inc.
Introduction
Speciation, the evolution of new species, is a central but un-
resolved issue in evolutionary biology.
(1)
What is the essence
of speciation? What geographical conditions are required for it
to happen? What evolutionary forces are crucial? Many
answers have been given to these questions and often appear
irreconcilable.
(2)
This has given rise to the conviction that
speciation is a very multifarious phenomenon, which defies
any generalisation. As I will argue in this paper, this confusion
stems largely from a conflict between two theories on specia-
tion that have existed side-by-side for the past sixty years. The
first of these theories is the one put forward by Charles Darwin
in 1859.
(3)
The second is the theory developed as part of the
Modern Synthesis in the 1930s and 1940s. Since the theories
differ chiefly in their emphasis on which factor drives popula-
tions apart, I will refer to them as the ``selection theory'' and the
``isolation theory'', respectively.
I will first recapitulate some aspects of the historical deve-
lopment of speciation theory, outline the basic tenets of both
views, and highlight the conflicts between them. Then I will
review three prominent debates related to speciation and
argue that all are reflections of those conflicts. At the same
time, I will describe recent data from field ecology, molecular
population genetics, laboratory experiments with Drosophila
and computer analysis, which suggest that a modernised
version of Darwin's view is more likely to bring progress in the
field than an emphasis only on the isolation theory.
The conflict
Species and speciation form the basis of one of the longest-
standing debates in biology. Dedicated attempts to define
species were made as early as the 17th century.
(4±6)
No single
early author, however, devoted as much time to it as Darwin,
whose expertise in taxonomy made him the foremost authority
on species in the mid-19th century. In On the Origin of Species
by Means of Natural Selection, he elaborated the point that
species are no more than ``well-marked varieties'', and that the
term was ``arbitrarily given for the sake of convenience to a set
of individuals closely resembling each other''.
(3)
He added that
the ``search for the undiscovered and undiscoverable essence
of the term species'' was in vain, as it was an attempt at
``defining the undefinable''.
(7)
Most present day biologists consider Darwin's opinion
outdated and mainly accept the ``biological species concept''
(BSC). The BSC, which was developed during the 1930s by
Ernst Mayr and Theodosius Dobzhansky, hinges (unlike
Darwin's concept) primarily on reproductive barriers. Mayr
defined species as ``groups of actually or potentially inter-
breeding natural populations, which are reproductively iso-
lated from other such groups''.
(8)
Dobzhansky consequently
applied the BSC to define the process by which species arise
(i.e., speciation) as ``that stage of the evolutionary process at
which the once actually or potentially interbreeding array of
forms becomes segregated into two or more separate arrays
which are physiologically incapable of breeding''.
(9)
1134 BioEssays 22.12 BioEssays 22:1134±1141, ß 2000 John Wiley & Sons, Inc.
Laboratory of Genetics, Wageningen University, Wageningen, The
Netherlands. Present address: Institute for Tropical Biology and
Conservation, Universiti Malaysia Sabah, Locked Bag 2073, 88999
Kota Kinabalu, Sabah, Malaysia. E-mail: schilthuizen@excite.com
Problems and paradigms