Reproductive mode and
speciation: the viviparity-driven
conflict hypothesis
David W. Zeh* and Jeanne A. Zeh
Summary
In birds and frogs, species pairs retain the capacity to
produce viable hybrids for tens of millions of years,
an order of magnitude longer than mammals. What
accounts for these differences in relative rates of pre-
and postzygotic isolation? We propose that reproduc-
tive mode is a critically important but previously over-
looked factor in the speciation process. Viviparity
creates a post-fertilization arena for genomic conflicts
absent in egg-laying species. With viviparity, conflict
can arise between: mothers and embryos; sibling
embryos in the womb, and maternal and paternal
genomes within individual embryos. Such intra- and
intergenomic conflicts result in perpetual antagonistic
coevolution, thereby accelerating interpopulation post-
zygotic isolation. In addition, by generating intrapopula-
tion genetic incompatibility, viviparity-driven conflict
favors polyandry and limits the potential for precopula-
tory divergence. Mammalian diversification is character-
ized by rapid evolution of incompatible feto-maternal
interactions, asymmetrical postzygotic isolation, dis-
proportionate effects of genomically-imprinted genes,
and ``F
2
hybrid enhancement.'' The viviparity-driven
conflict hypothesis provides a parsimonious explana-
tion for these patterns in mammalian evolution. BioEs-
says 22:938±946, 2000. ß 2000 John Wiley & Sons, Inc.
Introduction
How new species arise during evolution is one of the most
fundamental but highly contentious issues in biology.
Speciation occurs when populations diverge sufficiently to
become reproductively isolated; but is this isolation initiated
by pre-fertilization barriers to gene flow or by postzygotic
genetic incompatibility? There is currently little consensus
regarding the answer to this question, and much debate over
the relative importance of mutation accumulation, sexual
selection, selfish genetic elements and intergenomic conflict
in the speciation process.
(1±6)
With patterns in nature (see
below) exhibiting profound between-lineage differences in
the relative rates at which pre- and postzygotic isolation
evolve,
(7± 10)
a unifying theory of speciation has remained
elusive. Here, we present a new hypothesis to account for the
extreme disparity that exists between lineages in patterns of
speciation. This viviparity-driven conflict hypothesis proposes
that the reproductive stage at which divergence occurs most
rapidly between populations is strongly influenced by the
degree to which embryonic development involves physiolo-
gical interactions between mother and embryo. After briefly
reviewing between-lineage differences in patterns of specia-
tion, we develop the hypothesis that postzygotic isolation
should evolve more rapidly in viviparous animals than in
oviparous species, because development of the embryo
within the mother creates a physiological arena for genomic
conflicts absent in species that lay eggs.
Determining how reproductive isolation takes place, that
is, whether through mate choice and/or gametic barriers that
prevent fertilization or through the postzygotic mechanisms of
hybrid sterility or inviability, is fundamental to understanding
speciation.
(11±13)
As Coyne and Orr
(12)
point out, ``we would
like to know which type of isolation (pre- or postzygotic) is
most important in reducing gene flow between incipient
species, for this factor would be the primary component of
speciation.''
Speciation patterns in nature
By far the most comprehensive data set on speciation
patterns is derived from comparative studies of Drosophila
in which pre- and postzygotic divergence were found to occur
at similar rates.
(12)
However, in other lineages, this pattern
may not apply. For example, in birds, closely-related species
often differ most markedly in courtship behavior or in male
song and/or breeding plumage.
(14)
A similar pattern appears
to underlie the explosive diversification of African cichlids.
(15)
By contrast, in mammals, postzygotic incompatibility often
occurs without appreciable divergence in sexually-selected
traits.
(16)
Indeed, molecular assays
(7± 10)
strongly suggest
that the rate at which postzygotic incompatibility evolves
differs dramatically between lineages. As Fig. 1 illustrates,
bird and frog species pairs retain the capacity to produce
viable hybrid offspring for up to 60 million years, an order of
938 BioEssays 22.10 BioEssays 22:938±946, ß 2000 John Wiley & Sons, Inc.
Department of Biology and Program in Ecology, Evolution and
Conservation Biology, University of Nevada, Reno, Nevada.
Funding agency: National Science Foundation.
*Correspondence to: Dr. David W. Zeh, Dept. Biology & Program in
Ecology, Evolution and Conservation Biology, University of Nevada,
Reno, NV 89557. E-mail: zehd@unr.edu
Hypothesis