505
Crossing over does occur in males of Drosophila
ananassae from natural populations
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Beatriz Goñi, Muneo Matsuda, Masa-Toshi Yamamoto, Carlos R. Vilela, and
Yoshiko N. Tobari
Abstract: Spontaneous crossing over in males of Drosophila ananassae has been well demonstrated using F1 individuals
from crosses between marker stocks and wild type strains. However, the question of its occurrence in males from natural
populations remained open. Here we present the cytological evidence that crossing over does occur in males of D. ananassae from two Brazilian populations, sampled nearly 21 years apart, and in two recently sampled populations, one from Indonesia and one from Okinawa, Japan. Cytological analysis of meiosis in males collected from nature and in sons of females
from the same population inseminated in nature revealed the presence of chiasmata, inversion chiasmata, and isosite chromosome breakages in the diplotene cells in all sampled populations. These data demonstrate that reciprocal and nonreciprocal exchanges and chromosome breakages, previously reported as related events of male crossing over, do occur at variable
frequencies among males from natural populations.
Key words: meiotic chromosomes, chiasmata, chromosome breakages, Brazil, Indonesia, Japan.
Résumé : L’occurrence d’enjambements spontanés chez les mâles du Drosophila ananassae a été bien documentée au
moyen d’individus F1 issus de croisements entre des souches marquées et des souches sauvages. Cependant, la question de
son occurrence chez des mâles issus de populations naturelles demeure sans réponse. Dans ce travail, les auteurs présentent
des évidences cytologiques d’enjambements au sein de mâles du D. ananassae chez deux populations brésiliennes, échantillonnées à 21 ans d’écart, ainsi que deux populations échantillonnées récemment, l’une de l’Indonésie et l’autre d’Okinawa
au Japon. L’analyse cytologique de la méiose chez des mâles provenant des populations naturelles ou les fils de femelles
provenant de ces mêmes populations inséminées en nature a révélé la présence de chiasmas, de chiasmas typiques d’inversions et de cassures chromosomiques à des sites identiques chez les cellules en diplotène chez toutes les populations échantillonnées. Ces données démontrent que des échanges réciproques et non-réciproques ainsi que des cassures
chromosomiques, rapportés antérieurement comme étant des évènements apparentés survenant lors de la méiose chez les
mâles, surviennent à des fréquences variables chez les mâles provenant de populations naturelles.
Mots‐clés : chromosomes méiotiques, chiasmas, cassures chromosomiques, Brésil, Indonésie, Japon.
[Traduit par la Rédaction]
Introduction
Spontaneous crossing over in males of Drosophila ananassae was discovered by Kikkawa (1937) and Moriwaki (1938).
Both Kikkawa (1938) and Moriwaki (1940) reported that recombination in males of D. ananassae is controlled by chromosomal dominant enhancer genes, En(s) in chromosome 3
and En-II in chromosome 2. Since then, genetic elements
controlling male crossing over have been mapped on chromosomes 2 and 3 (Hinton 1970; Matsuda and Tobari 1983). All
data reviewed were obtained in crossing experiments carried
out in the laboratory using F1 males between marker stocks
and wild type flies collected from natural populations.
In 1983 Matsuda et al. succeeded in obtaining high quality
chromosome figures in male meiosis applying an air dry
method that permitted quantitative analysis. They demon-
Received 8 November 2011. Accepted 14 May 2012. Published at www.nrcresearchpress.com/gen on 12 July 2012.
Corresponding Editor: G. Jenkins.
B. Goñi* and Y.N. Tobari.† Department of Biology, Tokyo Metropolitan University, 1-1 Minami-Ohsawa, Hachioji, Tokyo 192-0397,
Japan.
M. Matsuda. Department of Biology, School of Medicine, Kyorin University, 6-20-2, Shinkawa, Mitaka, Tokyo 181-8611, Japan.
M.-T. Yamamoto. Drosophila Genetic Resource Center, Kyoto Institute of Technology, Saga-Ippongi-cho, Ukyo-ku, Kyoto 616-8354,
Japan.
C.R. Vilela. Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, Caixa Postal 11461,
São Paulo-SP, 05422-970, Brazil.
Corresponding author: M. Matsuda (matsudam@ks.kyorin-u.ac.jp).
*Present address: Sección Genética Evolutiva, Instituto de Biología, Facultad de Ciencias, Universidad de la República, Iguá 4225, 11400
Montevideo, Uruguay.
†Present address: The Research Institute of Evolutionary Biology, 2-4-28 Kamiyoga, Setagaya, Tokyo 158-0098, Japan.
Genome 55: 505–511 (2012)
doi:10.1139/G2012-037
Published by NRC Research Press
506
Genome, Vol. 55, 2012
Table 1. Collection sites and dates of Drosophila ananassae in Brazil, Indonesia (Java), and Japan (Okinawa).
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Collection sites
Date (m/y)
Brazil, São Paulo State
Rio Claro
June 1986
Ubatuba
June 1986
Ubatuba
July 2007
Caraguatatuba
July 2007
Guarujá
July 2007
Indonesia, West Java
Bogor
June 2008
Japan, Okinawa Prefecture
Naha
July 2008
Latitude and longitude
Collectors
22°24′39″S, 47°33′39″W
23°25′54.9″S, 47°04′17.5″W
23°25′54.8″S, 47°04′17.8″W
23°29′42.1″S, 45°08′25.5″W
23°58′32.8″S, 46°15′23.6″W
Alejo Mesa and Beatriz Goñi
Alejo Mesa and Beatriz Goñi
Francisca do Val and Beatriz Goñi
Francisca do Val and Beatriz Goñi
Francisca do Val and Beatriz Goñi
6°35′51″S, 106°47′54″E
Masato Kimura
26°12′44″N, 127°40′45″E
Masako Yafuso and Masanori Kondo
Table 2. Inversions found in four populations of Drosophila ananassae.a
Chromosome armb
Population
Brazil, 1986 (n = 23)c
Brazil, 2007 (n = 19)
Indonesia, 2008 (n = 22)
Japan, 2008 (n = 23)
XL
ST
ST
ST
ST
XR
ST
ST
ST
ST
2L
ST,
ST,
ST,
ST,
A
A
A, B, J
A
2R
ST, M, N, O
ST, M, N
ST, D
ST
3L
ST,
ST,
ST,
ST,
A
A
A
A
3R
ST,
ST,
ST,
ST,
A
A
A, N
A
Note: “A” refers to the following paracentric inversions known as cosmopolitan inversions: In(2L)A 22C;37C, In
(3L)A 64A;75, and In(3R)A 83C;87B. Additional paracentric inversions observed are In(2L)B 37D;41B, In(2L)J
21B;26C, In(2R)D 48C;53A, In(2R)M 51C;55B, In(2R)N 47C;56B, In(2R)O 48B;58D, and In(3R)N 92A;96A.
a
Tobari et al. 1993, Tomimura et al. 1993, and Y. Tomimura personal communication.
b
ST, A indicates segregation of the standard (ST) and the inversion (A).
c
Number of isofemale lines observed.
strated that chiasmata do occur in males at frequencies capable of accounting for the observed recombination values. Further cytogenetic studies revealed that the genetic factors
controlling male crossing over are involved in the origin of
exchange events and chromosome breakages (Goñi et al.
2006).
Whether crossing over in males living in natural populations occurs or not is an important issue for understanding
the role of genetic factors governing male crossing over in
population dynamics. This study presents the cytological evidence of crossing over and chromosomal aberrations in males
caught in natural populations in 1986, 2007, and 2008.
Materials and methods
Adult males of D. ananassae used in this study were collected in domestic habitats of three biogeographic regions:
Neotropical (Brazil), Oriental (Bogor, Indonesia), and Palearctic (Okinawa, Japan) in 1986, 2007, and 2008 (Table 1).
Flies were collected with an entomological net over fruits in
markets, orchards (decaying fruits), garbage dumps, and (or)
banana-baited traps. Adult males collected from nature and
sons of females inseminated in nature were used. All flies,
with the exception of flies from Brazil 2007 (which were cultured at uncontrolled room temperature), were cultured at
25 °C on the standard cornmeal, yeast, glucose, and agar medium.
Cytological analysis
Cytological preparations of testes were done individually
according to the method of Matsuda et al. (1983).
Results
Cytological evidence of crossing over in males from
nature
In general, 10% to 25% of the wild caught males processed
had primary spermatocytes at the diplotene stage. The number of diplotene cells scored for individual males ranged up
to 16 cells in the primary spermatocytes or to 32 cells in the
secondary spermatocytes per cyst. Meiotic chromosome configurations show two large similar metacentric pairs and a
tangled multivalent association formed by the X, Y, and 4th
chromosomes as previously reported (Hinton and Downs
1975; Matsuda et al. 1983, Tobari et al. 1993). The number
of chiasmata and of isosite chromosome breakages recorded
for the chromosomes 2 and 3 were combined as previously
done by Goñi et al. (2006).
Table 2 shows the gene arrangements found in the isofemale lines of the populations studied. Polytene nuclei show a
standard X chromosome, and the autosomes have three common cosmopolitan paracentric inversions, In(2L)A, In(3L)A,
and In(3R)A, and endemic paracentric inversion(s) (Tomimura et al. 1993; Y. Tomimura personal communication).
The cosmopolitan inversions have been found to be polymorphic in most of the geographically diverse populations. Males
heterozygous for large paracentric inversions, In(2L)A, In(3L)A,
are expected to form distinct meiotic inversion loop configurations in diplotene cells (Goñi et al. 2006) and can be
used as cytological markers in extended diplotene bivalents.
The presence of large paracentric inversion loops corresponding to the interstitial In(2L)A loop (see asterisk in
Figs. 1b, 1e, 2c, and 2f) and the distal In(3L)A “hook”
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Goñi et al.
507
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Fig. 1. Meiosis in males from Brazil (1986) (a–e) and Brazil (2007) (f). (a and f) Wild caught males and (b–e) sons of inseminated females.
Arrowheads in a–c indicate chiasmata. Arrowhead in d indicates an inversion chiasma with diagnostic U-type exchanges involving all chromatids and two acentric chromosome fragments, as graphically illustrated at right. Arrows in e and f indicate an isosite chromosome breakage
at proximal position. Asterisk in b, e, and f indicates chromosome inversion loops, involving the large interstitial In(2L)A loop (b and e) and
the large distal In(3L) “hook” loop (f). Multivalent association of the 4th, X, and Y chromosomes is indicated in e. Scale bar represents 5 µm.
loop (see asterisk in Fig. 1f) were observed in diplotene
cells of the males from all populations.
Chiasmata (Figs. 1a, 1b, 1c, 2a, and 2f) and inversion
chiasmata with diagnostic U-type exchanges (hereinafter referred to simply U-type exchanges) (Figs. 1d and 2d) were
observed in diplotene cells from most populations. U-type
exchanges show a crossing over within an inversion loop occurring in males heterozygous for inversions and thus included in the chiasmata counts (Goñi et al. 2006). U-type
exchanges resulted in chromosome bridge(s) and acentric
fragment(s) were found in the anaphase cells. However, chromosome fragments from U-type exchanges are sometimes
difficult to distinguish from those arising from isosite chromosome breakages in metaphase II and vice versa (Fig. 2e).
The term isosite was coined first by Matsuda et al. (1983) to
denominate “isosite chromosome aberration” in male meiosis
of D. ananassae including both U-type exchanges and chromosome breakages. Isosite exchange–breakages (Figs. 2a and
2b) involving chiasmata or inversion chiasmata and chromosome breakages at equivalent site on the bivalent are considered to be nonreciprocal exchanges (Goñi et al. 2006). These
events were observed in diplotene cells in some males from
natural populations (Supplementary data, Table S1)1. The
presence of reciprocal (chiasmata and inversion chiasmata)
1Supplementary
and nonreciprocal (isosite exchange–breakages) exchanges
observed in primary spermatocytes of D. ananassae from
natural populations demonstrates that crossing over does occur in males in nature.
Chromosome breakages (Figs. 1e and 1f) and isosite exchange–breakages (Figs. 2a and 2b) were observed in diplotene bivalents in males from nature (Table S1). Metaphase II
cells (Fig. 2e) with chromosome fragments were observed at
low frequencies in sons of inseminated females from two natural populations: 1.23% (4/314) from Brazil 1986, and 0.3%
(1/138) from Indonesia.
Chiasmata and isosite chromosome breakages relating to
crossing over in males from natural populations
Table 3 summarizes the cytological data of meiosis in wild
caught males and sons of wild caught females. Although, in
every population, chiasmata outnumbered isosite chromosome breakages by an average of 2.33 times and ranged
from 1.0 to 4.2 (Table 3), there was a positive correlation
(r = 0.574; df = 83, P < 0.001) between the two events using males with >8 spermatocytes (representing at least half
cyst per meiosis). Approximately 30% (n = 79/262) of the
sampled males had either chiasma(ta) and (or) isosite chromosome breakage(s) in every population, although the fre-
data are available with the article through the journal Web site (http://nrcresearchpress.com/doi/suppl/10.1139/g2012-037).
Published by NRC Research Press
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Fig. 2. Meiosis in males from Indonesia (a–e) and Okinawa (f). (a, b, and f) Wild caught males and (c and d) sons of inseminated females.
Arrowheads in a and f indicate chiasmata. Arrowhead in d indicates an asymmetric inversion chiasma as a result of a crossing over located laterally within the inversion loop; the persistent association of the acentric fragment at the site of the crossing over generates a U-shaped bivalent, as
graphically illustrated at right. In e, MII cell showing a chromosome fragment (arrow). Open arrow in a and b indicate isosite exchange–breakage
events in cells from the same (cyst) wild male from Indonesia: in a, acentric U-shaped fragment distally located and chromosome breakage, in b
proximal dicentric U-shaped exchange and chromosome breakage. Arrow in c indicates a isosite breakages on the 3R, as a characteristic In(2L)A
loop (asterisk) marks the bivalent corresponding to the chromosome 2. Asterisk in c and f indicates the In(2L)A loop. Scale bar represents 5 µm.
Fig. 3. Multidimensional scaling (MDS) plots of the distribution number of individual wild caught males (full circle) and sons of inseminated
females from wild populations (open circle) sorted by the frequency of chiasmata per cell for each population. Note the wide range and the
intermingled distribution of individual frequencies amongst the wild males and sons of inseminated females in most populations.
Published by NRC Research Press
56
314
40
138
27
316
4
32
3
8
3
25
19
0.13(0.03–0.28)
0.06(0.04–0.09)
0.09(0.03–0.35)
0.25(0.01–0.45)
0.10(0.03–0.50)
0.23(0.06–0.50)
1.9
3.8
Distributions of individual chiasma and (or) isosite
chromosome breakage in males from natural populations
Figure 3 shows the multidimensional scaling (MDS) plots
of the distribution number of wild caught males (full circle)
and sons of inseminated females from wild populations
(open circle) sorted by the number of cells examined and the
frequency of chiasmata and (or) isosite chromosome breakages per cell (Table S1). It shows a wide range of chiasmata
and (or) isosite breakages frequencies among the males examined. The distribution pattern of individuals within and
between populations supports a complex control of male
crossing over acting in natural populations, as previously reported in males from crosses using marker stocks.
5.7
0.08(0.04–0.25)
1.3
2.2
3.1
0.14(0.03–0.40)
2.5
1.4
quencies of males with either chiasmata and (or) isosite chromosome breakages vary from 14.3% to 46.1% among populations. The mean number of chiasmata per cell varied from
0.192 to 0.416 among populations (Table 3). On the basis of
the mean number of observed chiasmata per bivalent recorded in 34 males with >8 spermatocytes (n = 390 cells,
Table S2), we can estimate genetic crossing over: ranging
from 1.7% to 15.0% per chromosome. These results presented above agree with the recorded cytological data of
male crossing over using laboratory strains (Goñi et al.
2006).
144
Cells
observed
Males with >8 cells (n = 42)
4.2
12
50
133
16(39.9)
265
41
Wild caught males and sons of inseminated female from natural populations.
b
Half chiasmata or isosite exchange–breakages (see text) were counted as a single meiotic event.
a
2.9
5
9
6
35
29
233
44
429
7
52
3(42.9)
24(46.1)
1.0
1
7
0
8
3
90
26
355
7
54
1(14.3)
11(20.3)
103
489
18
83
3(16.7)
21(25.3)
27
184
5
31
2
22
1.5
Discussion
Brazil 1986
Wild caught
Sons
Brazil 2007
Wild caught
Sons
Indonesia
Wild caught
Sons
Okinawa
Sons
Males
analyzed
Cells
observed
n (%)
Cells
observed
Chiasmata
observed
Isosite chromosome
breakages observed
Chiasmata: isosite
chromosome
breakge ratio
All males (n = 79)
Bivalent (range)
Male
Bivalent (range)
Male
Mean number of chiasmata and (or) isosite chromosome
breakagesb per
Males with chiasmata and (or) isosite chromosome breakages
Primary spematocytes
Origin of
malesa
Table 3. Cytological analysis of male meiosis from four natural populations of Drosophila ananassae.
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Males
analyzed
509
Secondary spermatocytes
Goñi et al.
Previous studies examining crossing over in males of
D. ananassae were performed using heterozygous males resulting from crosses between marker stocks and wild type
strains. Based on these studies, male recombination in D. ananassae was shown to be produced from meiotic crossing over
and controlled by several genes, En, Su, and modifiers, as reviewed by Hinton and Downs (1975) and Matsuda et al.
(1993).
Kikkawa (1937) and Moriwaki (1938) found considerable
variation in recombination frequencies between strains. Tobari and Moriwaki (1973) studied male recombination using
140 males sampled from six Southeast Asian populations and
marker stocks. They found that 95% of males produced recombinants. In addition, they reported that the variation in recombination frequencies between individual males was
increased, ranging from 0 to 20% in the ebony–sepia interval
of the 2nd chromosome. These findings encouraged us to
study meiosis of males in natural populations. The present
study provides for the first time cytological evidence of
crossing over in males of D. ananassae in natural populations. We found an extensive variability in the frequency of
chiasmata and chromosome breakages among sampled males
from natural populations.
On the basis of the observed mean number of chiasmata
per bivalent recorded in males with >8 spermatocytes (34/
262), the expected genetic crossing over is ranging from
1.7% to 15.0% per chromosome (Table S2). Considering
these findings, genetic factors controlling male crossing over
are expected to be widely distributed and maintained in natural populations.
Natural populations of D. ananassae are highly polymorphic for three cosmopolitan inversions, In(2L)A, In(3L)A,
and In(3R)A (Table 2; Tomimura et al. 1993), and for enPublished by NRC Research Press
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510
hancers (En) and suppressors (Su) of male crossing over
(Hinton 1970; Matsuda and Tobari 1983, 1987). When crossing over occurs within the inversion loop, aberrant chromosomes can be produced (Goñi et al. 2006; the present study).
We found a positive correlation (r = 0.574; df = 83, P <
0.001) between frequencies of chiasmata and isosite aberrations in the present study. The effects of male crossing over
and of chromosome aberrations produced by U-type exchanges and isosite breakages on the population fitness remain to be studied.
As the male crossing over of D. ananassae is not the case
of hybrid dysgenesis (Goñi et al. 2006) it could be explained
by genes controlling male crossing over. The differences in
the frequencies of male recombination found in previous
studies and the variations found in chiasmata and chromosome aberrations observed in the present study might be explained by polymorphisms of inversions and enhancers (En)
and suppressors (Su) of male crossing over (Kikkawa 1938;
Moriwaki 1940; Hinton 1970, 1974; Matsuda and Tobari
1983, 1987; Tobari et al. 1980). Genetic factors controlling
crossing over in males of D. ananassae have been retained
in widespread populations, although the regulation of the
complex genetic system involving the function of En, Su,
and modifiers of male crossing over is not clear. Recently,
the whole genome sequencing of D. ananassae has been
completed (Clark et al. 2007; Schaeffer et al. 2008). This information will help us to analyze the molecular mechanisms
of male crossing over in D. ananassae.
In addition to the D. ananassae species subgroup, Franca
et al. (1968) reported low but significant rates of male recombination in Drosophila willistoni between two nonoverlapping paracentric inversions, so cytological evidence of
male crossing over has been searched for in this species (dos
Santos-Colares et al. 2003, 2006). dos Santos-Colares et al.
(2004) stated: “In a male larva of the population G3 (from
Arvoredo Island, Santa Catarina, Brazil), a heterozygote for
the inversion IIL-H, involving sections 53 to 55 in the distal
tip of the short arm of the second chromosome (da Cunha et
al. 1950), we observed in diplotene a probable consequence
of chiasma in the tip of IIL chromosomal arm, suggesting
the occurrence of recombination inside the inversion loop of
IIL-H”. Taking into account the preliminary male meiotic
data in D. willistoni and the widespread occurrence of male
crossing over in D. ananassae reported here, it seems worthwhile to test the current hypothesis on the mechanisms and
functions of meiotic exchange.
Acknowledgements
Cytological data (Brazil 1986) were also included in the
Ph.D. thesis of B.G., Tokyo Metropolitan University, 1989.
We thank A. Mesa (deceased), UNESP – Rio Claro, and F.
do Val, USP, for facilities during the field study in Brazil
1986 and 2007, respectively; M. Kimura, Hokkaido University, M. Yafuso, Ryukyu University, and M. Kondo, Kyusyu
University, for collecting flies from Indonesia and Okinawa;
Y. Tomimura for examining the polytene chromosomes; and
D.L. Pierce for kindly reading the manuscript. We are also
grateful to the anonymous reviewers for valuable comments.
This study was financed by the Japanese government (Monbukagakusho), CSIC – Universidad de la República and PEDECIBA (Uruguay), and the Drosophila Genetic Resource
Genome, Vol. 55, 2012
Center (Japan) to B.G. M.M. also thanks the National BioResource Project, Japan, for supporting and providing flies.
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