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A TEST OF THE CHROMOSOMAL REARRANGEMENT MODEL OF

SPECIATION IN DROSOPHILA PSEUDOOBSCURA


Author(s): Kirsten M. Brown, Lisa M. Burk, Loren M. Henagan, and Mohamed A. F. Noor
Source: Evolution, 58(8):1856-1860.
Published By: The Society for the Study of Evolution
DOI: http://dx.doi.org/10.1554/04-174
URL: http://www.bioone.org/doi/full/10.1554/04-174

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Evolution, 58(8), 2004, pp. 18561860

A TEST OF THE CHROMOSOMAL REARRANGEMENT MODEL OF SPECIATION IN


DROSOPHILA PSEUDOOBSCURA
KIRSTEN M. BROWN, LISA M. BURK, LOREN M. HENAGAN, AND MOHAMED A. F. NOOR1
Department of Biological Sciences, Louisiana State University, Life Sciences Bldg., Baton Rouge, Louisiana 70803
1 E-mail: mnoor@lsu.edu
Abstract. Recent studies suggest that chromosomal rearrangements play a significant role in speciation by preventing
recombination and maintaining species persistence despite interspecies gene flow. Factors conferring adaptation or
reproductive isolation are maintained in rearranged regions in the face of hybridization, while such factors are eliminated from collinear regions. As a direct test of this rearrangement model, we evaluated the genetic basis of hybrid
male sterility in a sympatric species pair, Drosophila pseudoobscura pseudoobscura and D. persimilis, and an allopatric
species pair, D. pseudoobscura bogotana and D. persimilis. Our results are consistent with the proposed model: virtually
all of the sterility factors in the former pair are associated with three inverted regions, whereas sterility factors are
present in the collinear regions in the latter pair. These findings indicate recombination and selection may have
eliminated sterility factors outside the inverted regions between D. p. pseudoobscura and D. persimilis, suggesting
chromosomal rearrangements may facilitate species persistence despite hybridization.
Key words.

Chromosomal inversions, Drosophila persimilis, Drosophila pseudoobscura, hybrid sterility, speciation.

Received March 12, 2004.

Because the process of speciation is rarely observed, we


strive to understand this process by surveying many pairs or
groups of taxa and identifying consistencies among them.
For example, cytogenetic studies in the last century proved
that closely related species were often fixed for different chromosomal rearrangements such as inversions or translocations
(Stebbins 1958; White 1969; King 1993). Researchers believed such rearrangements lead to meiotic disruptions in
heterozygotes (hybrids), and therefore contribute directly to
hybrid sterility. Although there is some support for this hypothesis (e.g., Gropp et al. 1982; Rieseberg et al. 1995;
Hauffe and Searle 1998; Delneri et al. 2003), two difficulties
with this proposal became apparent in the next several years.
First, new arrangements must have arisen in the heterozygous
state. If these new arrangements were strongly underdominant, they would have been immediately eliminated. Strong
genetic drift or meiotic drive (Walsh 1982) would be required
to allow a strongly underdominant new arrangement to
spread. If the new arrangements were only weakly underdominant, then they would not be significant contributors to
hybrid sterility. Second, several empirical studies of the fitness of rearrangement heterozygotes suggested that they are
often as fit, or nearly as fit, as homozygotes for an arrangement (Nachman and Myers 1989; Coyne et al. 1993; Reed
et al. 1995). As such, chromosomal speciation was considered largely untenable (Butlin 1993; Coyne 1994).
A few years ago, a new formulation of chromosomal speciation was introduced by Rieseberg (2001), Noor et al.
(2001a), and Navarro and Barton (2003a). These authors suggested that chromosomal rearrangements facilitate the persistence of hybridizing species because they lock together
sets of genes conferring adaptation or reproductive isolation,
and prevent them from breaking apart through recombination
in hybrids. Recombination had long been recognized as a
force that would facilitate the fusion of hybridizing taxa (e.g.,
Felsenstein 1981; Barton and Bengtsson 1986; Trickett and
Butlin 1994), but chromosomal rearrangements could inhibit

Accepted May 5, 2004.

recombination and avert fusion (see Ortz-Barrientos et al.


2002).
In support of this idea, Rieseberg et al (1999) showed that
rates of gene flow are higher between collinear than between
rearranged chromosomes in Helianthus sunflower hybrid
zones. Sixteen of the twenty-six rearranged segments were
also significantly associated with pollen sterility. Similarly,
in a literature survey of Drosophila species separated by hybrid sterility, Noor et al. (2001a) found that virtually all taxa
not separated by inversions were allopatric, whereas most
taxa differing by one or more inversions were sympatric,
suggesting inversions make the persistence of closely related
species more likely.
The North American species pair Drosophila pseudoobscura and D. persimilis has been studied extensively with
regard to the role of inversions in reproductive isolation and
species persistence. These species are separated by fixed or
nearly fixed paracentric inversions on three of their six chromosome arms spanning various lengths: of approximately
100 cytological bands across the genome, six cytological
bands are inverted on the left arm of the X-chromosome (XL),
11 cytological bands are inverted on the right arm of the Xchromosome (XR), and five cytological bands are inverted in
the center of the second chromosome (Tan 1935). However,
recombination still occurs across the uninverted regions of
these chromosomes (Dobzhansky and Tan 1936; Sturtevant
and Dobzhansky 1936; Noor and Smith 2000; Machado et
al. 2002). Noor et al. (2001a,b) found that all forms of reproductive isolation, and indeed other characters separating
these species (e.g., Noor and Coyne 1996; Williams et al.
2001), map almost exclusively to the three regions inverted
between them. Similarly, Machado et al (2002; Machado and
Hey 2003) found fixed DNA sequence differences in rearranged regions but extensive haplotype sharing in collinear
regions. Noor et al. (2001a) speculated that gene flow between D. pseudoobscura and D. persimilis eliminated or prevented the evolution of alleles conferring hybrid sterility between these species outside the rearranged regions.

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q 2004 The Society for the Study of Evolution. All rights reserved.

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TABLE 1. Fertility in pure-species and backcross hybrid males of


Drosophila pseudoobscura pseudoobscura (ps), D. p. bogotana
(bog), and D. persimilis (per). N1 denotes the total number of flies
dissected and genotyped. N2 indicates the number used for calculating the fraction fertile. Among the backcross hybrids, only those
homozygous/hemizygous for all three inversions from one species
were used for the calculation of fertility.
Males

FIG. 1. Estimated phylogeny of the Drosophila species studied.


The question mark indicates that hybridization between D. pseudoobscura and D. persimilis may have predated the split of D. p.
bogotana and D. p. pseudoobscura.

Here, we provide a direct test of the new chromosomal


speciation model. Drosophila pseudoobscura bogotana (hereafter, bog) occurs in Colombia and diverged from D. pseudoobscura pseudoobscura (hereafter, ps) approximately
150,000 years ago (see Fig. 1 and Schaeffer and Miller 1991).
These two subspecies bear the same sequence arrangements,
and thus also differ from D. persimilis (hereafter, per) by the
same three inversions. However, in contrast to ps, bog is
allopatric to per and has thus not hybridized with it at least
in the past 150,000 years. Therefore, we predict that bog and
per will be separated by alleles conferring hybrid sterility
both within and outside the inversions, whereas ps and per
will have all their sterility associated with alleles within inversions. Thus, the hybridization of bog and per effectively
acts as a negative control for the effect of sympatry and
hybridization in ps and per.
MATERIALS

AND

METHODS

N1

Pure species
bog ER
bog Sutatausa #5 strain
bog Susa #6 strain
per MSH 1993 strain
ps Flagstaff 1993 strain
ps James Reserve 032 strain
ps Mather 17 strain

101
100
100
137
164
131
108

N2

% Fertile

101
100
100
137
164
131
108

100
99
100
100
98
90
97

Backcross hybrids homo/hemizygous for all arrangements from one


species
68
88
483
Backcross to bog (ER)
64
64
451
Backcross to bog (Sutatausa #5)
74
46
494
Backcross to bog (Susa #6)
87
166
1147
Backcross to ps (Flagstaff 1993)
89
66
498
Backcross to ps (Mather 17)
93
28
532
Backcross to ps (JR032)

eclosion in groups of 530 individuals before fertility assays.


Approximately 500 males were scored from each backcross.
Fertility of pure strain males, F1 males, BCbog males, and
BCps males was assayed by dissection of testes in insect
Ringers solution using the method of Coyne (1984). A male
was scored as fertile if he had any motile sperm and sterile
if no motile sperm were observed. Although other means exist
for quantifying fertility (White-Cooper 2004), Coynes
(1984) method has been shown to be conservative (Campbell
and Noor 2001). Dissected males were frozen in labeled 0.6
ml microcentrifuge tubes.

Fly Stocks
All initial crosses were done to the D. persimilis line from
Mount St. Helena, California, collected in 1993 (see Noor
1995). The D. pseudoobscura lines used were Flagstaff 1993
(collected in 1993 from Flagstaff, Arizona), Mather 17 (collected in 1997 from Mather, California), and James Reserve
032 (collected from the James Reserve in southern California,
provided by Wyatt Anderson). The D. p. bogotana lines used
were Sutatausa #5, Susa #6 (both collected in 1997 by Diana
Alvarez), and a white-eye mutant subculture of the el Recreo
line (collected in 1978, provided by H. Allen Orr).
Crosses and fertility assays
Two classes of progeny were scored in this study: BCps
and BCbog, shortened from backcross to D. pseudoobscura and backcross to D. p. bogotana. BCps progeny were
generated by crossing females from a D. pseudoobscura line
to D. persimilis males, and backcrossing the F1 females to
the same D. pseudoobscura line. BCbog progeny were generated by crossing females from a D. p. bogotana line to D.
persimilis males, and backcrossing the F1 females to the same
D. p. bogotana line. All crosses were carried out at 20 6 18C,
85% relative humidity, on standard sugar/yeast/agar medium.
The male backcross progeny were aged for eight days after

Genotyping assays
Previously, we demonstrated that alleles at different loci
within the inverted regions do not recombine in F1 hybrid
females (Noor and Smith 2000). Therefore, in this study, we
only genotyped one microsatellite from within each inversion
for all backcross hybrid males. DNA was extracted using the
protocol of Gloor and Engels (1992). The following microsatellite markers were genotyped for the three chromosome
arms- XL: DPSX002 or runt; XR: DPSX010; and 2: bicoid.
Primer sequences and amplification conditions are published
(Noor et al. 2000; Noor et al. 2001b). PCRs were visualized
either on 2% TBE agarose gels or on acrylamide gels on a
LiCor 4200 DNA sequencer/analyzer. Genotypes were entered into StatView for data analysis.
RESULTS
Males from the inbred lines of the pure-species bore motile
sperm (hereafter, fertile; see Table 1). In contrast, at least
100 F1 males from every interspecies cross were scored, and
all of them without exception did not bear motile sperm (hereafter, sterile). Among backcross hybrid males (BCps and
BCbog), about 35% of males were fertile.
We limited our analyses to those backcross hybrid males

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FIG. 2. Predictions of genetic test presented here, where only backcross progeny homozygous or hemizygous for all three inversions
from the D. pseudoobscura subspecies were scored for fertility. The figure denotes the four major chromosomes of D. pseudoobscura
and D. persimilis. Inversions separating these species are indicated by ovals. Chromosomal regions derived from D. persimilis are presented
in grey, and D. pseudoobscura-derived chromosomal regions are presented in white. Regions that may have experienced recent natural
interspecies introgression are hatched. These introgressing areas include all the collinear autosomal regions derived from D. pseudoobscura
pseudoobscura and D. persimilis. Arrows denote example interactions between pairs of loci that might result in hybrid male sterility. (a)
Backcross to D. p. pseudoobscura (BCps). (b) Backcross to D. p. bogotana (BCbog).

that were homozygous or hemizygous for all three inversions


from ps or bog. If all hybrid sterility results from interactions
among alleles between inverted regions, then the resultant
males would be all or virtually all fertile. In contrast, if there
are alleles conferring sterility outside the inverted regions,
then several backcross hybrids will be sterile (Fig. 2).
Among BCps hybrid males, 8793% were fertile, suggesting little or no effect of genes in collinear regions on
hybrid male sterility. In fact, in the ps line from James Reserve, (nonsignificantly) more backcross hybrid males were
fertile than pure-species males. In contrast, among BCbog
hybrid males, 6474% were fertile, suggesting a substantial
effect of genes in collinear regions on hybrid male sterility.
The fertility difference between the BCps and BCbog lines
is statistically significant (Mann-Whitney U-test, P , 0.05).
Further, comparison between any individual BCps and any
individual BCbog line also showed significantly more sterility in the BCbog line (chi-square tests, P , 0.05).
DISCUSSION
Virtually all hybrid male sterility was associated with the
three inverted regions separating the hybridizing species pair
D. persimilis and D. pseudoobscura pseudoobscura. Backcross hybrids that were homozygous or hemizygous for all
three inverted regions from D. pseudoobscura were nearly all
fertile. In contrast, we found evidence of alleles conferring
hybrid male sterility in collinear regions of the allopatric
species pair D. persimilis and D. pseudoobscura bogotana.
Approximately one-third of hybrids homozygous or hemizygous for the three inverted regions from D. p. bogotana
were sterile. This difference is consistent with collinear re-

gions of the genome introgressing between D. p. pseudoobscura and D. persimilis, and hybrid-sterility-conferring alleles
being then eliminated from these regions. Introgression in
these collinear regions has been confirmed with DNA sequence data (Wang et al. 1997; Machado et al. 2002; Machado and Hey 2003; Hey and Nielsen 2004), and the present
study suggests a consequence of this introgression: loss of
factors conferring sterility. The inverted regions, however,
retain alleles conferring hybrid sterility and allow these species to persist.
The chromosomal rearrangement model test presented here
is robust to several possible evolutionary histories of these
taxa. Drosophila p. pseudoobscura and D. persimilis may have
been isolated through most of their divergence but came into
secondary contact after the split of D. p. pseudoobscura and
D. p. bogotana (see Fig. 1). Both the D. pseudoobscura subspecies would have borne alleles conferring sterility in hybridizations with D. persimilis, but such alleles in collinear
regions would have been eliminated by hybridization, recombination, and selection from D. p. pseudoobscura. An
alternative scenario could involve hybridization between D.
pseudoobscura and D. persimilis that predates the split of D.
p. pseudoobscura and D. p. bogotana. In that case, D. p.
pseudoobscura would have only accumulated alleles conferring sterility in its regions inverted relative to D. persimilis,
but D. p. bogotana accumulated such alleles in collinear regions only in its 150,000 years of isolation. These scenarios
can be distinguished through detailed examinations of the
sequences of sterility alleles separating D. p. bogotana and
D. persimilis that are currently present in collinear regions
of the genome.

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Three related models suggest how chromosomal rearrangements can facilitate species persistence through their effects
on recombination. Noor et al. (2001a) suggested that disadvantageous alleles (either through conferring differential
adaptation or reproductive isolation) would be eliminated after hybridization from collinear regions because of asymmetric effects: one allele might be disadvantageous in one
species while the alternate allele would be advantageous or
bear no cost in both species. As such, the former allele would
be eliminated while the latter would spread. In contrast, inverted regions, based on the large number of genes encompassed and linked, are more likely to bear multiple alleles
such that the whole region possesses a symmetric effect: one
allele disadvantageous in one species while the alternate allele is disadvantageous in the other species. Thus, neither
inversion can spread in a heterospecific genetic background.
Rieseberg (2001) independently proposed a very similar
model based on the summation of minor effects: inverted
regions are less likely to introgress between species than
collinear regions because the former may bear large number
of individual genes that each individually confer slight reproductive isolation or differential adaptation (Ortz-Barrientos et al. 2002). Finally, Navarro and Barton (2003a)
illustrated how advantageous alleles associated with incompatibilities between hybridizing populations would accumulate via a snowball process if associated with a nonrecombining barrier to introgression such as a chromosomal
rearrangement. These models make generally similar predictions, although Navarro and Bartons (2003a) model suggests
that incompatibilities are driven by positive selection and
predicts a molecular signature of natural selection in rearranged chromosomal regions (see Navarro and Barton
2003b).
Based on these models and our results, we hypothesize
mutations that confer hybrid male sterility between D. p.
pseudoobscura and D. persimilis arose in both inverted and
collinear regions of the genome. However, following hybridization, when such alleles introgressed between these
species, they were eliminated from collinear regions by recombination and natural selection. In contrast, sterility-conferring alleles were allowed to accumulate in collinear regions between D. p. bogotana and D. persimilis because these
species never hybridize. This contrast provides an elegant
negative control to the earlier observation of hybrid sterility being associated with inversions in D. p. pseudoobscura
and D. persimilis and supports a prediction unique to the three
new chromosomal speciation models.
Researchers have long known chromosomal rearrangements are associated with speciation or species persistence,
but the present results are more supportive of this association
resulting from the recombinational effects of rearrangements
rather than direct meiotic difficulties associated with rearrangements. Drosophila p. bogotana and D. p. pseudoobscura
are identical in chromosomal arrangement, so a meiotic model would not predict an excess of sterility in one of these
species over the other in hybridizations with D. persimilis.
Given the widespread pattern of species diversity with chromosomal rearrangements and the many observations of the
semipermeability of species boundaries (e.g., Harrison 1993;
Clarke et al. 1996; Butlin 1998; Jiang et al. 2000; Martinsen

et al. 2001; Besansky et al. 2003; Stre et al. 2003; Emelianov et al. 2004; Panithanarak et al. 2004), we postulate
that recombinational suppression may be a potent force in
preserving hybridizing sympatric species, and suggest the
model be tested across a broad taxonomic spectrum.
ACKNOWLEDGMENTS
This research was supported by a Howard Hughes Medical
Institute summer undergraduate research fellowship to KMB,
National Science Foundation grants 9980797, 0211007, and
0314552, and Louisiana Board of Regents Governors Biotechnology Initiative grant 005 to MAFN, and a Sigma Xi
grant-in-aid of research to LMH. We thank W. Anderson for
providing the strain from the James Reserve; H. A. Orr for
providing the mutant ER strain; S. D. Schully, R. Harrison,
C. Henzler, D. Ortz-Barrientos, L. Rieseberg, and an anonymous referee for constructive comments on this manuscript;
and L. Lohmiller and R. Beauvais for technical assistance.
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Corresponding Editor: R. Harrison

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