The American Society of Naturalists
Female Heterogamety in the Family Tephritidae (Acalyptratae, Diptera)
Author(s): Guy L. Bush
Source: The American Naturalist, Vol. 100, No. 911 (Mar. - Apr., 1966), pp. 119-126
Published by: The University of Chicago Press for The American Society of Naturalists
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Vol. 100, No. 911
The American Naturalist
March-April, 1966
FEMALE HETEROGAMETY IN THE FAMILY TEPHRITIDAE
(ACALYPTRATAE, DIPTERA)
GUY L. BUSH
Department of Genetics, University of Melbourne, Parkville, Victoria, Australia
An analysis of karyotypes in species representing three subfamilies of
Tephritidae has shown that sex determination by male heterogamety is
An XY system has been found in the
widespread in this family of flies.
olive fruit fly, Dacus oleae Gmel. of the Dacinae (Frizzi and Springhetti,
1953; Krimbas, 1963), and in several genera of fruit infesting Trypetinae
such as Anastrepha (Mendes, 1958; Bush, 1962), Rhagoletis (Bush, 1966a),
Zonosemata (Bush, 1966b), and Ceratitis (Mendes, 1958). Two species in
this subfamily, Anastrepha serpentine (Wied.) and Rhagoletis striatella v.d.
Wulp, are X1X2Y(Bush, 1962, 1966a). Finally, the gall-forming Spathulina
(Tephritis) arnicae (Linn.) of the subfamily Tephritinae is reported to be XO
It would appear, therefore, from earlier work that the
(Keuneke, 1924).
Tephritidae are no different from most other higher Diptera in their mechanism of sex determination.
Recently,
however, seven Australian species
of predominantly gallforming flies of the subfamily Tephritinae and one species belonging to the
Oedaspinae have been found to have female heterogamety.
Only one of
these species,
Chrysotrypanea tri/asciata Malloch, has been described;
another species belongs to the cosmopolitan genus Tephritis, while the remaining six species have been tentatively placed in three new genera.
This paper presents some preliminary observations on the cytology of
these flies and discusses the possible origin of female heterogamety.
MATERIALS AND METHODS
Satisfactory oogonial and spermatogonial divisions were obtained from
squashes of the developing gonads in the third larval instar, pupal, and
newly emerged adult stages.
Spermatogenesis in Chrysotrypanea tri/asciata
and NG-A sp. '1' was also studied in pupal and adult testes which had been
fixed in Navashin's fixative, sectioned and stained in Crystal Violet by
Newton's method. In the case of NG-B sp. '1', only adults which were
swept from what probably is its host plant have been available for study.
The species that have been examined are listed in Table 1.
RESULTS
The cytology of Ch. tri/asciata is representative of the species with female heterogamety. Details of the remaining species, including an analysis
of their polytene chromosomes and taxonomy, will be published at a later
date. At spermatogonial metaphase (Fig. 1) there are five pairs of metaand submetakinetic autosomes and an isomorphic pair of acro- or possibly
119
THE AMERICAN NATURALIST
120
TABLE 1
Species
of Tephritidae
Species
Host Plant
Tephritinae
Chrysotrypanea
trifasciata
Malloch
Compositae
Helichrysum dendroideum N. A. Wakefield (stem galls)
Ch. sp. '1'
Tephritis sp.
tit
1'(DC.)
New Genus-A
sp. '1'
New Genus-B
sp. '1'
NG-B sp. '2'
Oedaspinae
New Genus-C
sp. '1'
Date
Locality
Helichrysum sp.
(probably H. argophyllum (DC.)
(stem galls)
Olearia pimeleoides
(flower
heads)
0. phlogopappa
(Lab.) (stem galls)
0. lirata (Sims)
NG-A sp. '2'
examined.
Wilsons Promontory, Vic. Dec. 21, 1964
Sherbrooke Fst. (vic.
Dec. 26, 1964
of Fern Tree Gully),
Vic.
Carey's Peak, Barrington Feb. 13, 1965
Tops State Fst.,
N.S.W.
4 mi. S Whyalla, S.A.
Aug. 7, 1965
5 mi. E Marysville, Vic.
Mt. Baw Baw & Mt.
Donna Buang, Vic.
Nov. 24, 1964
Various dates:
Nov. 30,
1964 to May
10, 1965
Mar. 9, 1965
Cape Otway, lighthouse
rd., Vic.
21 mi. NE Cowell, S.A.
0. lepidophylla
July 12, &
Aug. 7, 1965
(Pers.) (stem galls)
8 mi. E Noojee, Vic.
Cassinia longifolia
Dec. 14, 1964
R.Br. (stem galls)
H. dendroideum
Wilson's Promontory, Vic. Dec. 21, 1964
(sweeping only)
Goodeniaceae
Goodenia ovata Sm.
Wilson's Promontory, Vic. Dec. 21 & Dec.
(stem galls)
Olinda, Vic.
26, 1964
The Z-chromosomes in the male
subacrokinetic
sex chromosomes (ZZ).
show less tendency toward somatic pairing than do the autosomes, and are
All species show
often found widely separated in squash preparations.
this
same
basic
pattern
in the male.
A study
of meiosis
in squashes
and
sectioned material has shown that typical achiasmatic bivalents are formed
at first metaphase.
There is, therefore, no crossing-over in the male. With
the exception of Megaselia scalaris (Phoridae) (Mainx, 1965), achiasmatic
meiosis in the male is a feature common to all the higher Diptera whose
cytogenetics have been investigated in some detail (White, 1954).
At oogonial
metaphase
there
are five
pairs
of meta-
and submetakinetic
autosomes, plus a single acro- or subacrokinetic Z-chromosome and a small
dot W-chromosome (Fig. 2). In other species the W-chromosome takes the
form of a dot (Chrysotrypanea
sp. '1'; NG-A
sp. '1'), a short rod (Tephritis
sp. '1' and sp. '2'; NG-B sp. '1'; NG-C sp. '1'), or a large metakinetic
(NG-B sp. '2').
Chrysotrypanea, NG-A, and NG-C have fair to good polytene chromosomes
in the adult and pupal Malpighian tubules.
Usually fair to poor polytene
chromosomes were found in the salivary glands of the third larval instar,
whereas the best preparations came from cells in the posterior region of the
121
IN FLIES
SEX CHROMOSOMES
bf~~F42
~~~~~~~~~
3
25P
.
4
25;
FIGS. 1-2. Spermatogonial (1) and oogonial (2) metaphase plates of Cbrysotrypanea trifasciata Malloch.
FIGS. 3-4. Polytene chromosomes from posterior mid-gut region of NG-C sp. '1'
(3) and NG-A sp. '1' (4).
The parental homologues may be either
mid-gut and Malpighian tubules.
paired as in NG-C (Fig. 3) or unpaired as in NG-A (Fig. 4). Chromosomes
of larval, pupal, and adult Malpighian tubules of Tephritis sp. '1' and
NG-B, however, are too poor for detailed study. As yet no inversions have
been found in three species whose polytene chromosomes have been studied
in a number of individuals.
DISCUSSION
The occurrence of female heterogamety in Diptera is not restricted to the
Tephritidae but is also present in a somewhat rudimentary form in the
monogenic species Chrysomyia albiceps and C. rufifacies (Calliphoridae)
(Ullerich, 1963) which produce unisexual broods. Gynogenic females (?producing) are heterozygous for a potent female sex-realizer Ff, whereas
androgenic females (&-producing) and males are homozygous ff. The males
have no influence in sex determination and there is no indication of genetiwell differentiated sex chromosomes; consequently,
cally or cytologically
Such monogenic spethere is probably no need for dosage compensation.
cies may represent recent shifts from male to female heterogamety in which
a balance between male and female determiners has not yet reached an
equilibrium.
THE AMERICAN NATURALIST
122
Sex determination in certain monogenic Sciaridae (Metz, 1938) and possibly some Cecidomyidae (White, 1950) may be somewhat similar but complicated by the presence of an extremely bizarre meiotic cycle.
Some form of
dosage compensation appears to be necessary in these species since males
are XO in the somatic line and both males and females are XX in the germ
line.
Female heterogamety has also recently been discovered in a single species of Chironomidae.
Martin (1965) found that females of Polypedilum
nubifer (Skuse) were heterozygous for a heterochromatic tip in the polytene
chromosomes of the salivary gland while the majority of males were hoMartin considers that the occurrence of occamozygous for its absence.
sional heterozygous males indicates that there are either a number of male
and female determining genes in the population of varying potency, or that
the heterochromatic end does not include the female sex determining gene
but is closely linked to it. The fact that heterogametic males do occur suggests, as pointed out by Martin (1965), that P. nubi/er is probably in the
process of changing from male to female heterogamety.
Other Diptera are heterogametic in the male and, at least on a theoretical
basis, may be classified into five basic types with respect to the sex determining role of the autosomes and sex chromosomes (Table 2). In species possessing
one of the Y types, the Y-chromosome is male determining
and sex depends on a balance between male determiners on the Y-chromosome
and female determiners on the X-chromosome, the autosomes, or on both the
X-chromosome and autosomes.
However, it should be stressed that although
TABLE 2
Possible types of sex determining mechanisms in male and female heterogametic
animals. m = male-determining; f = female-determining; o = neutral. This represents
the over-all sex determining potency of the chromosomes and does not exclude the
possibility of both male and female determiners occurring in the same chromosome.
Male Heterogamety
~~SexofXO
individuals
3'
2AoXf Xf
2Afxfxf
2Af XoXo
2Af XmXm
2AmXfXf
2AoXfYm
2Af Xf Ym
2Af XoYm
2Af Xmym
2AmXfYo
metac3
Tp
Type
Y/X
Y/XA
Y/At
YX/A
X/A
"ty
e"
types
Female Heterogamety
Sex of ZO
individuals
Type
2AoZmWf
2AmZmWf
2AmZOWf
2A0ZmZM
2AmZmZm
2AmZoZO
3'
3'
2AmZf wf
2AmZf zf
meta-S
WZ/A
2Af ZMWO
2Af ZmZm
?
Z/A
W/Z
W/ZA
W/A I
types
IN FLIES
SEX CHROMOSOMES
123
the Y-chromosome is known to be male determining in several Diptera
(Ullerich, 1963; Ullerich, Bauer, and Dietz, 1964; Mainx, 1965) as well as
man and probably all other mammals (White, 1960), the nature of the relationship between the Y and other chromosomes, as proposed in Table 2,
Some of these types
has not been definitely established for any species.
may therefore never or only rarely occur in nature.
In some Diptera, such as the Chironomidae and Megaselia, the X and Y
are homologous except for a single or possibly two or more closely linked
This "simple" system of sex determination has apparently evolved
loci.
from more primitive Diptera which have what is normally considered a rather
system with visibly different X and Y chromosomes (White,
specialized
in the
1964). Why homology between the X and Y has been reestablished
It seems apparent, howChironomidae and Megaselia is not at all clear.
ever, that the development of a system of sex determination in which the sex
chromosomes are well differentiated is not necessarily a one-way process.
Although female XO individuals have been noted in at least one Dipteran
species of the Y type (Ullerich, 1963), XO species can only exist as a result of a fusion between the Y and an autosome or the X. Males may appear
to be cytologically XO, but are genetically XY or XYY (White, 1954). It
should also be possible for YO species to evolve from a Y/A type (i.e.,
species with one more chromosome in the male than in the female karyotype). These could be genetically XX?, XXY&. No YO species have in
fact been recorded in the many hundreds of animals investigated cytologiof the XY relationcally thus far. Because of the inherent characteristics
is
therefore always
and
holandrically
ships where only the Y is inherited
On the
occur.
never
may
X,
they
the
by
selection
shielded from direct
surveys;
in
not
cytological
checked
often
are
other hand, female karyotypes
so the existence of YO species cannot be entirely ruled out.
Dosaige compensation in certain Y type species could be entirely absent
and sex determination relatively simple. This is probably the case in the
phorid Megaselia scalaris (Mainx, 1965) and some Chironomidae (Beermann,
1955; Martin, 1962) in which the Y differs from the X only in the presence
of a male sex-realizer or chromosomal rearrangement. It could also be more
complicated in such species as Pales /erruginea (Tipulidae) (Ullerich,
Bauer, and Dietz, 1964) and Phormia regina (Calliphoridae) (Ullerich, 1963)
which possess distinct heteromorphic X and Y chromosomes, and therefore
Such species could
probably require some means of dosage compensation.
be any one of the four Y types.
The X/A type of sex determination involves a balance between femaledeterminers on the X-chromosome and male-determiners on the autosomes.
The Y-chromosome has no influence over sex determination; thus, XO individuals are male. Cytologically and genetically XOS'-XX? species can
and do exist in some Drosophila and possibly exist in a few other Diptera
including the tephritid Spathulina arnicae (Keuneke, 1924; Patterson and
Stone, 1952; Ullerich, Bauer, and Dietz, 1964). It seems likely that the
X/A system which requires some sort of dosage compensation represents a
124
THE AMERICANNATURALIST
type of sex determining mechanism in the Diptera that
rather specialized
has been derived from one of the Y types.
Whether a Z/A or one of the W types of sex determination outlined in
Table 2, as well as dosage compensation, occurs in the female heterogametic
Chrysotrypanea and related genera is not known. The occurrence of distinct
of difheteromorphic sex chromosomes indicates the possible existence
This would suggest
ferential regions between the Z and W chromosomes.
that some sort of dosage compensation is present, and also that a considerable amount of cytogenetical evolution has occurred since the original
It seems unlikely that this shift
shift from male to female heterogamety.
occurred as a one-step process in an X/A or Y type species with well differentiated sex chromosomes and well developed mechanisms for dosage
Such species require a highly integrated genome of sex decompensation.
and compensating genes (Cock, 1964) which untermining, sex-linked,
It would
doubtedly represents the product of a long evolutionary history.
therefore be difficult, if not impossible, for a single mutation involving sex
It is more likely
reversal in an X/A species to be adaptive immediately.
that the shift took place as a result of small changes in the potency of sex
determining genes in a species of the Y/X or Y/XA type, which had only
slight differences in the genetic constitution of the sex chromosomes and
no elaborate mechanism for dosage compensation.
The occurrence of female heterogamety in both the Tephritinae and
Oedaspinae at first glance would indicate a common origin. This conclusion is also supported by the fact that certain tribes in both groups appear
to be closely related on morphological grounds. They are similar in general
habitus, wing pattern, structure of the head and male and female genitalia,
position and type of thoracic setae and bristles, and gall-forming habits.
On the other hand, the reported case of male heterogamety in Spathulina
arnicae, also of the Tephritinae, suggests that either the subfamilial classification does not represent true relationships or that female heterogamety
has arisen independently on several occasions within the family. It is also
possible that the species in question has been misidentified and should be
checked again. The answer to these questions will have to await a careful
survey and study of the sex determining mechanisms in the Tephritidae.
Such an investigation should also furnish additional information on the intergeneric and interspecific relationships and evolution within the family.
SUMMARY
Female heterogamety has been found in eight Australian species of
Tephritidae belonging to Chrysotrypanea, Tephritis, and three new genera.
Evidence suggests that female heterogamety evolved in response to selection through small potency changes in species of the Y/X or Y/XA types
which lacked elaborate mechanisms for dosage compensation.
ACKNOWL EDGMENTS
I would like to thank Prof. M. J. D. White for his helpful suggestions in
this investigation and for reading and discussing the manuscript with me. I
SEX CHROMOSOMES IN FLIES
125
would also like to express my appreciation to Mr. Ray Smith of the National
Herbarium of Victoria for kindly identifying the host plants.
This investigation was supported in part by a Public Health Service fellowship 1-F2-GM-20,
289-01, Sigma Xi, and the American Philosophical Society.
LITERATURE
CITED
und Evolution genetischen
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