A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation.
Abstract
The role of chromosomal inversions in adaptation and speciation is controversial.
Historically, inversions were thought to contribute to these processes either by directly
causing hybrid sterility or by facilitating the maintenance of co-adapted gene complexes.
Because inversions suppress recombination when heterozygous, a recently proposed local
adaptation mechanism predicts that they will spread if they capture alleles at multiple
loci involved in divergent adaptation to contrasting environments. Many empirical
studies have found inversion polymorphisms linked to putatively adaptive phenotypes
or distributed along environmental clines. However, direct involvement of an inversion
in local adaptation and consequent ecological reproductive isolation has not to our
knowledge been demonstrated in nature. In this study, we discovered that a chromosomal
inversion polymorphism is geographically widespread, and we test the extent to which
it contributes to adaptation and reproductive isolation under natural field conditions.
Replicated crosses between the prezygotically reproductively isolated annual and perennial
ecotypes of the yellow monkeyflower, Mimulus guttatus, revealed that alternative chromosomal
inversion arrangements are associated with life-history divergence over thousands
of kilometers across North America. The inversion polymorphism affected adaptive flowering
time divergence and other morphological traits in all replicated crosses between four
pairs of annual and perennial populations. To determine if the inversion contributes
to adaptation and reproductive isolation in natural populations, we conducted a novel
reciprocal transplant experiment involving outbred lines, where alternative arrangements
of the inversion were reciprocally introgressed into the genetic backgrounds of each
ecotype. Our results demonstrate for the first time in nature the contribution of
an inversion to adaptation, an annual/perennial life-history shift, and multiple reproductive
isolating barriers. These results are consistent with the local adaptation mechanism
being responsible for the distribution of the two inversion arrangements across the
geographic range of M. guttatus and that locally adaptive inversion effects contribute
directly to reproductive isolation. Such a mechanism may be partially responsible
for the observation that closely related species often differ by multiple chromosomal
rearrangements.
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https://hdl.handle.net/10161/4449Published Version (Please cite this version)
10.1371/journal.pbio.1000500Publication Info
Lowry, David B; & Willis, John H (2010). A widespread chromosomal inversion polymorphism contributes to a major life-history
transition, local adaptation, and reproductive isolation. PLoS Biol, 8(9). pp. e1000500. 10.1371/journal.pbio.1000500. Retrieved from https://hdl.handle.net/10161/4449.This is constructed from limited available data and may be imprecise. To cite this
article, please review & use the official citation provided by the journal.
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Show full item recordScholars@Duke
John H. Willis
Professor of Biology
We conduct research on broad issues in
evolutionary genetics, and we
are currently addressing questions relating to
the evolution of adaptation, reproductive isolation,
breeding systems, inbreeding depression, and
floral traits in natural plant populations.
Please see our lab web page for more
information.

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