PARTHENOGENESIS THROUGH FIVE GENERATIONS IN THE SCORPION LIOCHELES AUSTRALASIAE (FABRICIUS 1775) (SCORPIONES, ISCHNURIDAE)

2005·5 MB·English

by  Kazunori Yamazaki

2004. The Journal of Arachnology 32:852-856
SHORT COMMUNICATION
PARTHENOGENESIS THROUGH FIVE GENERATIONS
IN THE SCORPION LIOCHELES AUSTRALASIAE
(FABRICIUS 1775) (SCORPIONES, ISCHNURIDAE)
Kazunori Yamazaki^: Institute of Life and Environmental Sciences, University of
Tsukuba, Tsukuba, Ibaraki 305-8572, Japan
Toshiki Makioka^: Institute of Biological Sciences, University of Tsukuba, Tsukuba,
Ibaraki 305-8572, Japan
ABSTRACT, Females of Liocheles aiistralasiae (Fabricius 1775) collected from a maleless population
on Iriomote Island, Ryukyu, Japan, and separately reared in the laboratory have parthenogenetically pro-
duced five successive generations in seven years. Many individuals ofthe first generation collected in July
1994, gave birth to the second generations from 1994-1998, and some of the second generation gave
birth to the third generation from 1997-1999. The fourth generations were born from 1999-2001, and the
fifth generations were born in January-August 2001. Most females of all generations gave birth to about
20 neonates after approximately an eight-month pregnancy. In the ovary of a fourth generation female,
as well as in those of most ofthe second generation females, there were growing embryos and a number
of oocytes of various sizes, suggesting a possibility of the sixth generation or subsequent generations by
parthenogenesis.
Keywords: Thelytokous parthenogenesis, successive generations, histological section
Among 1259 scorpion species described in the thiesen 1962, 1971; San Martin & Gambardella
world (Fet etal. 2000), thelytokous parthenogenesis 1966) and T. bolivianus uruguayensis (Borelli
has been reported only in seven species (Matthiesen 1900) (Zolessi 1985) and an ischnurid, Liocheles
1962, 1971; San Martin & Gambardella 1966; Mak- australasiae (Fabricius 1775) (Makioka 1993).
i1o9k9a1;&LKoouirkeengo198&4,C1u9e8l5l;arZo1l9e9s4s;i 1M9a8k5i;oLkoaur1e9n9g3o; thrMeaettihnideisveindua(l1s962o)fftohuendseicnoTnidtyugsenseerrartuiloant,usbtohrant
Maury 1997; Lourengo et al. 2000). In some of from the first field-collected generation, partheno-
these species, parthenogenesis has been presumed genetically gave birth to the third generations when
based on the absence of males in the populations reared separately. Later he reported that one ofthe
(Lourengo 1991; Lourengo & Cuellar 1994), female third generation individuals, reared separately, gave
biased sex ratios (Maury 1997) and all female ne- birth to a total of 33 fourth generation offspring
onates (Lourengo 1991; Lourengo & Cuellar 1999). (Matthiesen 1971). In T. serrulatus, San Martin &
However, one ofthe best evidences ofparthenogen- Gambardella (1966) also reported that two second
esis is an achievement of independent rearing, i.e., generation females gave birth to 22 third generation
being raised alone without the presence of males, offspring, only two of which gave birth to eight
through successive generations. In only three scor- fourth generation offspring. Zolessi (1985) stated
pion species, has parthenogenesis been confirmed that, for T. bolivianus uruguayensis he successively
by means of independent rearing through three or obtained second andthirdgenerations whenfemales
fbuotuhridssu,ccTeistsyiuvsesegrennielraattuisonLsu;tzth&isMwealslose1e9n22in(Mtawto- wneurmeberresaroefdmostehpearrastealnyd, nbeuotnahtees.diIdnLniootchsehleoswautsh-e
tralasiae Makioka (1993) obtained many third gen-
' Present address: Department of Biological Sci- eration offspring under separate rearing conditions.
ences, Graduate School of Science, University of In these previous works, however, only afew ofthe
Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, second or third generations produced offspring par-
Japan. ticularly in the Tityus species, and no neonates of
2Present address: 4-31-13 Kitami, Setagaya, Tokyo the third or the fourth generations became mature
157-0067, Japan. to produce offspring, leaving unanswered the ques-
852
YAMAZAKI & MAKIOKA—PARTHENOGENESIS IN A AUSTRALASIAE 853
—
Figure 1. Separate rearing in Liocheles australasiae. Scale = 2 cm.
tion as to whether parthenogenesis is an evolution- the fourth generation that experienced parturition
ary strategy in these species or whether the phe- once were dissected in physiological saline solution
nomenon is limited to only a few generations. In for histological observations. The ovaries were re-
the present study, we have attempted to answerthis moved, fixed with Bouin’s solution, dehydrated in
question inL. australasiae by rearing them through a graded ethanol-n-butaeol series, embeddedinpar-
more than four generations. affin and serially sectioned at 5 fxm thickness. The
A total of413 females ofLiocheles australasiae sections were stained with Mayer’s hematoxylin
were collected from a maleless population (Mak- and eosin, and the number of oocytes, embryos
ioka & Koike 1984, 1985; Makioka 1992a, 1992b, growing in the ovarian diverticula, and empty ovar-
1993) on Iriomote Island, one of the Ryukyu Is- ian diverticula (remnants of previous parturitions)
lands, Japan, in July 1994. These specimens are de- was counted under a light microscope.
posited in the collections ofthe Biological Sciences A total of 147 ofthe 413 first-generation females
ofUniversity ofTsukuba (TKB-anim. 1008-1421). experienced 165 parturitions to produce 1118 sec-
First generations derived from the collected speci- ond generation offspring during the period from
mens were serially numbered and kept separate in 1994-1998. From these second generation off-
mm mm
glass vials (27 in diameter and 55 in spring, 46 females became mature and experienced
height) with a piece of wet filter paper (Fig. 1) at 98 parturitions to produce 493 third generation off-
28 ± 1 °C in adarkincubator, andfedtermites once spring, 19 of which experienced 28 parturitions to
a week. produce 180 fourth generation offspring. From the
The firstinstarjuveniles ofthe secondgeneration fourth generations, only seven females became ma-
bom from those females immediately climbed onto ture and gave birth to 78 fifth generation offspring
their mother’s back, stayed there without eating for through six parturitions.
about a week (Fig. 2), and then molted into second The ovary of each female dissected consisted of
instarjuveniles (Fig. 3) which left their mother and threelongitudinal andfourtransverseovariantubes,
took food by themselves. Each ofthe second instar which bore many growing ovarian diverticula con-
juveniles was kept separatein anew glass vial soon taining oocytes or embryos and empty ovarian di-
after the first molt, and serially numbered. Theju- verticula which had lost their embryos in the pre-
veniles were fed termites once a week, the number vious parturitions. In adult ovaries, as described in
of which was varied with the scorpion’s instar. We previous papers (Makioka 1992a; Yamazaki &
took special care not to give soldier termites to the Makioka 2001), there were neither oogonia nor oo-
young scorpions, because the soldiers canwoundor cytes in the walls of the ovarian tubes and all the
kill young scorpions. All specimens were watered oocytes were contained in their own ovarian diver-
daily and their conditions (molt, parturition, death, ticula, waiting to develop into embryos.
etc.) were checked and recorded. In the ovary of the fourth generation female ex-
Ten females of the second generation that expe- amined immediately after her death, there were 20
rienced parturitions at least once and a female of large empty ovarian diverticula that had newly lost
.
854 THE JOURNAL OF ARACHNOLOGY
—
Figure 2-3. First instarjuveniles of Lioclieles aiistrakisiae mounted on their mother’s back. Scale =
1 cm. 3. Second instarjuveniles ofLiochelesaiistralasiae immediately afterthe first molton theirmother’s
back. Scale = cm.
1
their embryos at the last parturition (Fig. 4) and 86 between 20 empty ovarian diverticula and 18 neo-
smaller ovarian diverticula containing oocytes of nates counted at birth, may have been eaten by the
various sizes (Fig. 5). No growing ovarian divertic- mother (see Polis & Sissom 1990). Neither male
ula containing growing embryos were found. Two gonadal tissues, such as ovotestes, nor sperm re-
neonates corresponding to the difference in number ceiving structures, such as spermathecae, were
—
Figures 4-5. Ovarian sections ofthe fourth generation in Liochelesaiistralasiae 4. Ovariandiverticula
containing a primary oocyte (arrows) and empty ovarian diverticula (ed). ot, ovarian tube. Scale: 500 pm.
5. Enlargement of small ovarian diverticula containing primary oocyte (po). f; follicle epithelium. Scale
= 50 pm.
YAMAZAKI & MAKIOKA—PARTHENOGENESIS IN L. AUSTRALASIAE 855
found in the ovaries of the second and the fourth Brown, C.A. 1997. Growth rates in the scorpion
generation females. Pseudouroctonus reddelli (Scorpionida, Vaejov-
Some authors have attempted to rear scorpions idae). Journal of Arachnology 25:288-294.
from neonates to adults in order to ascertain their Fet, V., Sissom, W.D., Lowe, G, & Braunwalder,
life histories (Rosin & Shulov 1963; Smith 1966; M.E. 2000. Catalog of the Scorpions of the
Matthiesen 1970; Francke 1976; Sissom & Francke World (1758-1998). New York Entomological
1983; Francke & Sissom 1984; Benton 1991; Society, New York, 690 p.
Brown 1997) and to confirm parthenogenetic repro- Francke, O.E 1976. Observations on the lifehistory
duction (Matthiesen 1962, 1971; San Martin & of Uroctonus mordaxThorell (Scorpionida, Vae-
Gambardella 1966; Zolessi 1985; Makioka 1993; jovidae). Bulletin of the British Arachnologigal
Lourengo & Cuellar 1999). In most cases, however, Society 3:254-260.
none or only a few of neonates reached the adult Francke, O.E & Sissom, WD. 1984. Comparative
&
stage (Matthiesen 1962, 1970, 1971; Rosin Shu- review of the methods used to determine the
lov 1963; San Martin & Gambardella 1966; Smith numberofmolts to maturity in scorpions (Arach-
1966; Francke 1976; Sissom & Francke 1983; nida), with analysis of the post-birth develop-
France & Sissom 1984; Zolessi 1985; Benton 1991; ment of Vaejovis coahuilae Williams (Vaejovi-
Brown 1997). Among them, only three partheno- dae). Journal of Arachnology 12:1-20.
genetic scorpions successivelycontinuedtoproduce Lourengo, W.R. 1991. Parthenogenesis in the scor-
csounbdsietqiuoennst(gMeantetrhaiteisoenns 1u9n6d2e,r1t9h7e1;seSpaarnatMearrteianrin&g pBuitohnidTaiet)y.usBuclolletuimnbioafntuhse B(rTihtoirsehllA)ra(cShcnoorlpoigoinceas:l
Gambardella 1966; Zolessi 1985; Makioka 1993). Society 8:274-276.
Matthiesen (1971) succeeded in obtaining 33 ne- Lourengo, W.R. & Cuellar, O. 1994. Notes on the
onates of the fourth generation from a mother of
geography ofparthenogenetic scorpions. Biogeo-
the third generation in Tityus serrulatus andZolessi
graphica 70:19-23.
(1985) obtained an unspecified number ofneonates Lourengo, W.R. & Cuellar, O. 1999. A new all-fe-
of the third generation from the second generation
male scorpion and the first probable case of ar-
in T. bolivianus uruguayensis, but they did not
rhenotoky in scorpions. Journal of Arachnology
mention the fates of these neonates. In Liocheles
27:149-153.
onauefsottnrhaaetleassseicoaofen,tdhMegaektnhieiorrakdtaigoe(nn1,e9r9ba3ut)tioornbetafarriionngmedwfaoausnrutmmhobetnehreterorsf- LouCrueelnlgaor,, OW..2R0.0,0.CAloruedvsileewy-ofThpoamrtphseonno,genJe.sLi.s i&n
minated by an incubator accident. Thereafter, in scorpions with a description of postembryonic
1994, we began the present study and have suc- development in Tityus metuendus (Scorpiones,
ceeded in obtaining a number ofindividuals offive Buthidae) from western amazomia. Zoologischer
successive generations of L. australasiae. At pres- anzeiger 239:267-276.
ent, 78 second instars of the fifth generation are Makioka, T. 1992a. Reproductive biology ofthe vi-
being raised. At the same time, in a fourth gener- viparous scorpion, Liocheles australasiae (Fabri-
ation female after the first parturition, the ovary cius) (Arachnida, Scorpiones, Ischnuridae). II.
contained a number of oocytes of various sizes. It Repeatedpregnancies in virgins. InvertebrateRe-
seems likely therefore, that the present specimens production and Development 21:161-166.
of L. australasiae will continue to reproduce par- Makioka, T. 1992b. Reproductive biology ofthe vi-
thenogenetically through further generations under viparous scorpion, Liocheles australasiae (Fabri-
the present laboratory conditions, as well as in their cius) (Arachnida, Scorpiones, Ischnuridae). III.
native population of Iriomote Island, and that our Structural types and functional phases of the
separate rearing method is well suited to L. austra- adult ovary. Invertebrate Reproduction and De-
lasiae. We suggest that because of the number of velopment 21:207-214.
offspring produced by parthenogenesis and because Makioka, T. 1993. Reproductive biology of the vi-
of the number of generations we have now reared, viparous scorpion, Liocheles australasiae (Fabri-
parthenogenesis is indeed a stable reproductive cius) (Arachnida, Scorpiones, Ischnuridae). IV.
strategy in this species. Pregnancy in females isolated from infancy, with
We wish to thank Dr. Koji Tojo, University of notes onjuvenile stage duration. InvertebrateRe-
Tsukuba, for his helpful advice on preparing the production and Development 24:207-212.
presentpaper. We alsothankDr. Hiroshi Ando,Tsu- Makioka, T. & Koike, K. 1984. Parthenogenesis in
rumi University, and Mr. Yuji Takayama and Mr.
the viviparous scorpion, Liocheles australasiae.
Hiroyuki Mitsumoto, University of Tsukuba, for Proceedings of the Japan Academy 60, series B,
their assistance in collecting andrearing specimens.
No. 9:374-376.
LITERATURE CITED Makioka, T. & Koike, K. 1985. Reproductive bi-
Benton, TG. 1991. The life history of Euscorpius ology of the viviparous scorpion, Liocheles aus-
flavicaudis (Scorpiones, Chactidae). Journal of tralasiae (Fabricius) (Arachnida, Scorpiones,
Arachnology 19:105-110. Scorpionidae). I. Absence of males in two natu-
856 THE JOURNAL OF ARACHNOLOGY
ral populations. International Journal of Inverte- San Martin, P.R. & De Gambardella, L. A, 1966,
brateReproductionandDevelopment8:317-323. Nueva comprobacion de lapartenogenesis en TT
Matthiesen, F.A. 1962, Parthenogenesis in scorpi- tyus serrulatus Lutz y Mello-Campos 1922
ons, Evolution 16:255-256, (Scoipionida, Buthidae). Revista de la Sociedad
Matthiesen, F.A. 1970. Le developpement post-em- de Entomologia de Argentina 28:79-84.
bryonnaire du scorpion Buthidae: Tityus bahien- Sissom, W.D. & Francke, O.E 1983. Post-birth de-
sis (Perty, 1834), Bulletin du Museum National velopment of Vaejovis bilineatus Pocock (Scor-
d’Histoire Naturelle, Paris 41:1367-1370. piones: Vaejovidae). Journal ofArachnology 11:
Matthiesen, F.A. 1971. The breeding of Tityus ser- 69-75.
&
rulatus Lutz Mello, 1927, in captivity (Scor- Smith, G.T. 1966. Observations on the life history
pions, Buthidae). Revista rasileira de pesquisas of the scorpion Urodacus abruptus Pocock
medicas e Biologicas 4:299-300. (Scorpionidae), and an analysis ofits home sites,
Maury, E.A. 1997. Tityus trivittatus en la Argenti- Australian Journal of Zoology, 14:383-398.
na. Nuevos dates sobre distribucion, partheno- Yamazaki, K. & Makioka, T. 2001. Ovarian struc-
genesis, sinantropia y peligrosidad (Scorpiones, tural features reflecting repeated pregnancies and
Buthidae). Revista del Museo Argentine de
parturitions in a viviparous scorpion, Liocheles
Ciencias Naturales “Bernardino Rivadavia” 24:
australasiae. Zoological Science, 18:277-282.
1-24.
Polis, G.A. & Sissom, W.D. 1990. Life history. Pp. Zolessi, L.C. 1985. La partenogenesis en el escor-
pion amarillo Tityus bolivianus uruguayensis
161-223. In Biology of Scorpions. (G.A. Polis,
(Borelli, 1900) (Scorpionida: Buthidae). Actasde
ed.). Stanford University Press, Stanford, Cali-
las Jomadas de Zoologia del Uruguay 13-14.
fornia.
Rosin, R. & Shulov, A. 1963. Studies on the scor-
pion Nebo hierochonticus. Proceedings of Zoo- Manuscript received 18 March 2002, revised 22
logical Society ofLondon 140:547-575. October 2003.