Drosophila Males Contribute to Oogenesis in a Multiple Mating Species
Author(s): Therese A. Markow and Paul F. Ankney
Source: Science, New Series, Vol. 224, No. 4646 (Apr. 20, 1984), pp. 302-303
Published by: American Association for the Advancement of Science
Stable URL: http://www.jstor.org/stable/1692140
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tion of segregationice and frozen sedi- DrosophilaMales Contributeto Oogenesisin a
mentsmay representannualtemperature
cycles, although this type of stratifica- MultipleMating Species
tion can also occur under constant temperatureconditions.
Abstract. Two species of Drosophila that diffierin their ecology and mating
Because formationof segregationice systems have been comparedwithrespect to male contributionto the somatic tissues
involves drawing additional water into and developing oocytes offemales. In the species Drosophilamojavensisfemales
the system, and because segregationice remate daily, exhibita copulatoryplug, and have been shown to obtain a contribucan continue to form even under great tion from the male ejaculate. In contrast, Drosophilamelanogastermales do not
pressure,ice islandheightsof 7 m are not contributetofemales. Female Drosophilamelanogasterdo not remateasfrequently
unexpected. At most lakes, the islands as Drosophilamojavensisfemales nor is a copulatoryplugformed.
probably were even higher in the past
Species of Drosophilashow wide vari- tributenutrientsto oocytes andto female
and definitelywere largerin area. These
ice deposits are now disappearing,and ability in matingsystems (1). One of the somatic tissues while D. melanogaster
the most spectacularones, such as those most strikingdifferencesobserved is the males apparentlydo not.
Males were isotopically labeled by
at Laguna Colorada, will probably not frequency at which females of various
persist for more than a decade or two. species remate. For example, mated fe- placingfreshly oviposited eggs on CaroHowever, their future will be strongly males of the cosmopolitan species D. lina instantDrosophilamediumcontaininfluencedby even small changes in lake melanogaster,when providedwith males ing 3H-labeledamino acids (4). Virgin
water level, air temperature,or geother- every morning, usually will not remate males were separatedupon eclosion and
for about S to 7 days (2). Under similar stored at 24° + 1°C until they were remal activity.
H. HURLBERTconditions, females of the SonoranDes- quired for mating experiments. After 4
STUART
ert endemic cactiphilicspecies D. moja- days, labeled D. melanogaster males
Department of Biology,
vensis rematedaily. The patternof daily were matedto unlabeledfemales. Whole
San Diego State University,
remating in D. mojavensis is observed D. melanogastermales showed an averSan Diego, California 92182
C. Y. CHANG even when matedfemales do not ovipos- age of 28,509 disintegrationsper minute
CECILY
it and even thoughthe ventralreceptacle at the time of mating.Labeled D. mojaWater Resources Division,
may containnumeroussperm(1). Anoth- vensis males were stored for 8 days
U.S. Geological Survey,
er differencebetween these two species beforebeing matedto unlabeledfemales;
Menlo Park, California 94025
is the formation of a reaction mass or these males showed an averageof about
copulatory plug following mating in D. 350,000 disintegrationsper minute. The
Referencesand Notes
1. G. E. Stoertz and G. E. Ericksen, U.S. Geol. mojavensis but not in D. melanogaster developmentaltime of D. mofavensis is
Surv.Prof. Pap. 811(1974).
(3). The evolutionarysignificanceof this 50 percentlongerthanD. melanogaster,
2. O. Ballivianand F. Risacher,Los Salares del
which most likely accountsfor the larger
AltiplanoBoliviano(Officede RechercheScien- differencein rematingfrequency is postifiqueet TechniqueOutre-Mer,Paris, 1981).
size of D. mojavensis and their higher
to
an
interspecific
be
linked
to
tulated
3. T. Vila, Rev. Geol. Chile2, 41 (1975).
4. F. Ahfeld,Geologiade Bolivia(Los Amigosdel difference in parental investment by
concentrationof radioactivity.The presLibro,La Paz, 1972).
5. M. Servant and J. C. Fontes, Cah. ORSTOM males (I); specifically, D. modavensis ence of isotope in mated females was
Ser. Geol. 10, 9 (1978).
females, living in a harsh environment determinedimmediatelyafter copulation
6. Salinity of melted ice samples from this and
otherlakes rangesfromless than 1 to 3 per mil, often with limitedresources, are predict- and again 24 hours later (5). The body
with few exceptions.Determinationsmadewith ed to remate more frequentlyin orderto
parts analyzed are shown in Table 1.
an AmericanOpticalhandrefractometer(model
In both species a large amount of
obtainnutrientsfrom the male ejaculate.
10419).
7. F. C. Walcott,Geogr.Rev. 15, 346 (1925).
was seen in the female reradioactivity
during
that,
evidence
We
now
present
8. J. H. MercerandO. PalaciosM., Geology5, 600
(1977) S. Hastenrath The Glaciation of the copulation,males of D. mojavensisconproductivetract(uterus,ventralreceptaEcuajorian Andes (Baikema,Rotterdam,1981)G. H. Dentonand W. Karlen,Quat.Res. (N. Y.)
3, 155 (1973);H. H. Lamb, Palaeogeogr. Palaeoclim.Palaeoecol. 1, 13 (1965).
9. S. Taber,J. Geol. 38, 303 (1930);J. R. Mackay,
Can.J. EarthSci. 10 979 (1973),Geogr.Bull. 8
59 (1966);in Proceedingsof the 2nd International Conferenceon Permafrost(NationalAcademy of Sciences, Washington,D.C., 1973), p.
223;A. L. Washburn,Geocryology(Wiley,New
York, 1980).
10. At fourwidely separatedpoints in this lake, the
salinityof lake waterrangedfrom 146to 292 per
mil; salinity of pore water from 0.5 m beneath
the lake bottomrangedfrom5 to 15 per mil.
11. S. Hurlbertand C. Chang, Proc. Natl. Acad.
Sci. U.S.A. 80, 4766 (1983).
12. We thank G. Bejarano and the Ministry of
Agricultureof Boliviaandnumerouscivilianand
militaryauthoritiesin both Boliviaand Chilefor
facilitatingour work. For assistance and companionshipin the field we thank especially E.
Berna, J. Berna, J. Berna, A. Gonzalez, J.
Keith, M. Lopez, C. Mitchell, H. Marcos, L.
Pena, T. Saire, and A. Vargas. AlejandroBarrero and personnelof MinaLagunaVerde providedinvaluablelogisticalsupport.R. Berry,R.
Lowe, S. Sitko, A. Sturz, and J. VeRaillie
analyzedsedimentand water samples.This paperis dedicatedto Sr. AlejandroBarreroDelgado, pioneerexplorerof the Sud Lipez. Supported by grants from the National Geographic
Society.
20 January1984;accepted22 February1984
302
Table 1. Radioactivityfound in females at two times aftermating.Datapresentedare averages
for single females. At least three replicationsof three females per replicationwere performed
for each time point. Countsper minutewere convertedto disintegrationsper minuteaccording
to a standardquench curve. Controls consisted of body parts from unlabeledfemales. The
results are given as means + standarderrors.
Radioactivity(disintegrationsper minute)
Part
Head
Thorax
Abdoment
Reproductivetract
Ovarianeggs
Head
Thorax
Abdomen
Reproductivetract
Ovarianeggs
0 hours
-
24 hours
Drosophilamelanogaster
23.8 +
18.9 + 0.8
31.1 +
23.7 + 4.6
25.1 +
39.5 + 12.2
50.4 +
1112.4 + 63.1t
23.9 +
25.9 + 9.8
Drosophilamodavensis
56.23 +
31.6 + 6.6
98.0 +
50.4 + 8.6
72.2 +
28.9 + 6.4
67.4 +
1426.7 + 118.6t
191.7 +
32.2 + 8.5
t*
6.1
8.7
3.1
23.9
5.4
1.39
1.31
1.09
6.47§
0.32
3.6t
5.5t
5.3t
9.1t
20.4t
5.2111
7.77§
10.24§
84.44§
8.622§
*Whenappropriate,the Welch methodwas used (11); otherwisetwo-tailedt-tests were used to compare
tDiffers significantly from unlabeled conSMinus reproductive tracts.
sample means.
IIP< 0.05.
§P < 0.01.
trols.
SCIENCE,VOL. 224
cle, and spermathecae)immediatelyafter copulation.At this point the amount
of isotope in other parts did not differ
significantlyfrom that in control. Twenty-four hours later a large amount of
isotope still remainedin the reproductive
tracts, although the level was reduced.
In D. melanogasterfemalesradioactivity
decreased in the reproductivetract, and
no significantamounts of isotope were
detected in any other tissues after 24
hours. Drosophila females have been
observed to expel material from their
reproductivetract after mating (6), and
we have assumed that this accounts for
the reduction in the amount of isotope
after 24 hours.
However, D. modavensis females
showed significantradioactivityin other
body parts, especially unfertilizedovarian oocytes. Since oogenesis requiresapproximatelythe same length of time in
both these species, and the same female
reproductivestate existed in both experiments, differential rates of oogenesis
cannot be the underlying cause of the
presence of isotope in D. mojavensis
oocytes. The amount of isotope also
increases in the somatic tissues of-D.
modavensisfemales within 24 hours. The
molecularnatureof the substancestransferred is still unknown, but since male
contributionhas also been documented
with l4C-labeled amino acids (7) any
major role of tritium exchange in the
observation of male contributionin D.
mojavensiscan be ruled out.
After two or three consecutive matings, D. melanogastermales are temporarily sterile (2, 8). This sterility is
caused by a reductionin male accessory
gland secretions, not by a reduction in
spermnumber.After 24 hours, abstinent
males regain their fertility (2). In contrast, D. modavensis males may mate
seven or more times consecutively without any observable reductionin fertility
(1). It is possible that D. modavensis
males transferless materialat each copulation in order to take advantageof the
increased mating opportunitiesin their
population.
The phenomenonof males transferring
nutrientsto females whichthen appearin
female somatic tissues and oocytes has
been demonstratedin several species of
Lepidoptera(7). In these two Drosophila
species, which differin theirecology and
mating systems, a difference in male
contribution to egg production is also
apparent. Drosophila melanogaster, a
cosmopolitan species, can use a variety
of substratesfor breeding.However, D.
modavensis uses necrotic tissue of organ
pipe cactus in Sonora, Mexico and
20 APRIL 1984
449 (1978); G. Lefevre and U. B. Jonsson,
southern Arizona, and agria cactus in
Genetics47, 1719(1962).
Baja California.At certain times of the
3. J. T. PattersonandW. S. Stone,Evolutionin the
Genus Drosophila (Macmillan, New York,
year these resources are limited, and
1952).
even duringtimes of abundantresources 4. Fifty eggs were placed in shell vials containing
1.5 g of food mediummade up with 50 ,uCiof a
females are selective aboutthe stage and
mixtureof 3H-labeledaminoacids (ICN20063).
conditionof the necrotictissue on which 5. Body partsfromthree femaleswere pooled in a
singlescintillationvial containing100,ulof Scinthey will oviposit (9). Females must be
tiGest tissue solubilizer.Tissues were crushed
with glass rods and allowed to digest for 24
able to manufactureeggs and also surhours at 50°C. Glacial acetic acid (2.5 61) was
vive until findingan appropriateplace to
addedto neutralizethe solution.Five mllliliters
of
ScintiVerseI scintillationfluidwas then addoviposit, and male nutrientcontribution
ed, and each vial was allowed to sit for an
may help them do this. The discovery of
additional24 hours.
M. H. Gromkoet al., in SpermCompetftionin
male nutrient contribution ln a genus 6. Insects,
R. L. Smith, Ed. (Academic Press,
whose phylogenetic relationships are
New York, in press);R. F. Rockwell, personal
communication;W. B. Heed, personalcommuwell defined, whose mating systems
nication.
vary, and whose ecology is under inten- 7. C. L. Boggs and L. E. Gilbert,Science 206, 83
(1979) C. L. Boggs Evolution35, 931 (1981);
sive study (10) provides a new opportuand W. B. *att, Oecologia (Berlin)50,
320 (1981).
nity to inquireinto the evolution of mat8. T. A. Markow, M. Quaid, S. Kerr, Nature
ing strategiesin insects.
(London)276, 821 (1978).
9. W. B Heed, personalcommunication.
THERESE
A. MARKOW 10.
J. S. F. Barker and W. T. Starmer, Eds.,
PAULF. ANKNEY
EcologicalGeneticsand Evolution:TheCactusYeast-DrosophilaModel System (Academic
Departmentof Zoology,
Press, Sydney, 1982); B. Shorrocks, in The
Genetics and Biology of Drosophila, M. AshArizonaState University,
burner, H. L. Carson, J. N. Thompson, Jr.,
Tempe85287
Eds. (AcademicPress, London, 1982)vol. 3b
Referencesand Notes
1. T. A. Markow,in Ecological Geneticsand Evolution: The Cactus-Yeast-DrosophilaModel
System,J. S. F. BarkerandW. T. Starmer,Eds.
(AcademicPress, Sydney, 1982);Anim.Behav.,
in press.
2. D. W. Pyle and M. H. Gromko,Experientia34,
pp. 385-425; M. Begon, in ibid., pp. 345-381,
M. Ashburner,in ibid., vol. 3a, pp. 375-421.
11. G. W. Snedecorand W. G. Cochran,Statistical
Methods(Iowa State Univ. Press, Ames, 1967),
p. 115.
12. We thankDrs. RobertGemmillandCarolBoggs
for technical advice. Supportedby NIH grant
GM30638-01(T.A.M.).
24 October1983;accepted 23 January1984
MonoclonalAntibodyto Thy-1 EnhancesRegenerationof
Processesby Rat Retinal GanglionCells in Culture
Abstract. Ganglioncells were dissociatedfrompostnatal rat retinas identifiedby
specific fluorescent labels and maintained in culture on a variety of substrates.
Regeneration of processes by retinal ganglion cells was enhanced when the cells
were plated on glass coated with a monoclonalantibodyagainst the Thy-l determinant. Plain glass and glass coated with polylysine, collagen, fibronectin, or other
monoclonal antibodies supported the growth of neural processes, but were less
efective than antibodyto Thy-l.
Detailed studies of differentiatedmammalianneuronswould be aidedby examining identified cells in vitro. This approach requires that viable cells be isolated, unequivocallyidentified,and cultured. Like other neurons of the central
nervous system (CNS), mammalianretinal ganglioncells normallydo not regenerate their axons after transection, and
indeed many of the cells degenerate(1).
It is important, therefore, to know
whether differentiated retinal ganglion
cells can surviveand regenerateprocesses in culture.
Since ganglion cells are the only retinal cells that projectto otherareas of the
CNS, they can be labeled by retrograde
transportof markersinjected into their
projection sites, such: as the superior
colliculus and lateral geniculate nucleus
(2). In histological sections Thy-1 anti-
gen is located on cells and processes in
the inner retina and can be used to
specificallyidentify the ganglioncells in
vitro (2, 3). Thy-1 is also expressed on
the surfaceof manyneuronsnot found in
the retina as well as on T lymphocytes
and embryonic muscle (4). Because of
sequence homology with immunoglobulins, it has been suggested that molecules displayingthe Thy-1 antigenplay a
role in cellular recognitionand morphogenesis in the nervous system (4).
In this report we describe aspects of
the identificationand growth of solitary
rat retinalganglioncells in culture. MacLeish et al. (S) observedthat salamander
neurons could be grown and maintained
on antibody-coatedglass cover slips; we
tried this method with several antibodE
ies. Comparinggrowth on differentsubstrates, we found that, by the second day
303