FINE STRUCTURE OF MALE GENITAL SYSTEM AND SPERM IN SOLIFUGAE DOES NOT SUPPORT A SISTER-GROUP RELATIONSHIP WITH PSEUDOSCORPIONES (ARACHNIDA)

7 Pages·2002·9.6 MB·English

by  G Alberti

2002. The Journal of Arachnology 30:268-274
FINE STRUCTURE OF MALE GENITAL SYSTEM AND SPERM
IN SOLIFUGAE DOES NOT SUPPORT A SISTER-GROUP
RELATIONSHIP WITH PSEUDOSCORPIONES (ARACHNIDA)
G. Alberti: Zoologisches Institut u. Museum, Ernst-Moritz-Arndt^Universitat, J.=S.-
Bach-Str.l 1/12, D-17489 Greifswald, Germany. E-mail: [email protected]
A. V. Peretti: Catedra de Diversidad Animal I, Universidad Nacional de Cordoba,
Av. Velez Sarsfield 299, 5000 Cordoba, Argentina
ABSTRACT. Comparative spermatology may provide characteristics that can be useful in systematics.
Previous observations on sperm structure of the solifugid Eusimonia mirabilis revealed that the most
similar arachnid sperm cells are found within the Actinotrichida (Acari). The general morphology of the
testis and the tendency to form sperm aggregates are also similar in both taxa. Since knowledge of sperm
in Solifugae until now came only from one species, in contrast to Acari in which all the higher taxa have
been investigated, these characters were difficult to assess with regard to systematical implications. The
present paper confirms the derived, simple-aflagellate structure of sperm in Solifugae and the similarity
with sperm of Actinotrichida, presenting results for two further species of another family (Ammotrechidae)
from Argentina. Sperm cells of representatives of both taxa are small, devoid of a flagellum, contain a
chromatin body that is penetrated and surrounded by circles of the acrosomal filament, and have a tendency
to form peripheral protuberances. Sperm morphology does not support the frequently suggested sister-
group relationship between Solifugae and Pseudoscorpiones.
Keywords: Arachnid sperm, comparative spermatology, sperm aggregates, systematics
Solifugae present a number of peculiar has frequently been suggested or discussed in
characteristics that are considered to repre- the past, but it has never really been accepted
sent a mixture of plesiomorphies and auta- (e.g. Hammen 1989; Evans 1992). Hammen
pomorphies (Moritz 1993). Hence the posi- (1989), who considered the Acari as being
tion of Solifugae within the Arachnida and diphyletic, created two taxa Apatellata (Pseu-
their relationship with other taxa is difficult doscorpiones and Solifugae) and Epimerata
to define. Nevertheless, most authors who (Palpigradi and Actinotrichida), which he
have considered the phylogenetic systematics placed into a sister-group relationship. Dun-
of Arachnida regard Solifugae as most close- lop (2000) recently accepted the sister-group
ly related to Pseudoscorpiones (e.g. Wey- relationship between Solifugae and Pseudo-
goldt & Paulus 1979a, b; Hammen 1989; scorpiones (forming the Haplocnemata) and
&
Shultz 1990; Wheeler Hayashi 1998; Wey- suggested Acari as the possible sister group
goldt 1998). However, this putative sister- of Haplocnemata.
group relationship is based on only a few In general, phylogenetic relationships with-
characteristics of debatable value, e.g. rostro- in the Arachnida are still at least partly con-
soma, two-jointed chelicerae and segmenta- troversial. Hence, further characteristics are
tion of the legs (Shultz 1990; Moritz 1993). evidently necessary to improve or falsify sug-
A
relationship between Solifugae and Acari gested concepts. Comparative spermatology
—
Figures 1, 2. Transmission electron micrographs. 1. Oltacola gomezi (Solifugae, Ammotrechidae), one
group of sperm embedded in germinal layer. At left, glandular tissue. Scale bar = 2 (jim. 2. Oltacola
gomezE detail of seminal vesicle. Scale bar = lp,m. Abbreviations: BL = basal lamina, GB = Golgi body,
GC = glandular cell, M = mitochondrion, MU = muscle, MV = microvilli, N = nucleus, SC = somatic
cells, SD = septate desmosome, SE = secretion, SP = sperm cells.
268
ALBERTI & PERETTI—MALE GENITAL SYSTEM AND SPERM IN SOLIFUGAE 269
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270 THE JOURNAL OF ARACHNOLOGY
may provide such characteristics (Jamieson A wide seminal vesicle and a pair of long, thin
1987; Alberti 2000). testes is present on each side.
The only spermatozoa of Solifugae for Each testis is composed of a spermatogenic
which the fine structure has been described are part (germinal layer) and a glandular part that
those of Eusimonia mirabilis Roewer 1934 differ strikingly (Fig. 1). The germinal layer
(Karschiidae) from Morocco (Alberti 1980a). comprises somatic cells that form a meshwork
Contrary to descriptions based on light mi- in which groups of mature sperm cells are em-
croscopy (Roewer 1934), it was shown that bedded. We did not find earlier stages of sper-
they are highly derivative and differ strikingly matogenesis. The larger part of the testis is
from those of Pseudoscorpiones, which pre- composed of a glandular epithelium that pro-
sent a coiled-flagellate type of sperm and thus duces the secretions, predominantly proteinic,
are more plesiomorphic (Alberti 1995, 2000). found in the narrow testicular lumen and most
The sperm ultrastructure of E. mirabilis shows likely present also in the seminal vesicle.
apomorphic similarities with sperm of actin- The vesicle wall is composed of a flat epi-
otrichid mites (Alberti 1980a, b, 2000). The thelium underlain by a few muscle cells (Fig.
present paper intends to broaden our knowl- 2). The wide lumen of the vesicle is filled with
edge of the spermatological characteristics of secretions and groups of sperm cells. The se-
Solifugae in order to establish whether the re- cretions differ according to the species. In O.
sults obtained from the single previously in- gomezi there are distinct globules embedded
vestigated species apply more generally to this in a homogeneous matrix, whereas such glob-
peculiar order. ules are less obvious in P. patagonicus. The
METHODS difference between these secretions may ex-
plain an observation during the fixation pro-
The following species, both belonging to
cess: in P. patagonicus the tissue in each spec-
the family Ammotrechidae, were used for this
imen changed colour, whereas in O. gomezi
study: Procleobis patagonicus (Holmberg
this did not happen.
1876) and Oltacola gomezi Roewer 1934.
The groups of sperm cells are highly or-
Specimens were captured in San Jose de las
dered in E. mirabilis, forming piles of regu-
Salinas, Cordoba, Argentina. After dissection,
they were fixed in ice-cold 3.5% glutaralde- larly arranged sperm cells (Figs. 5, 8). In both
the species from Argentina, these groups are
hyde buffered in Sorensen phosphate buffer
less complex. In O. gomezi, the spermatozoa
(pH 7.4; 0. IM). They were then mailed in di-
luted glutaraldehyde to Germany, where fur- collectively form distinct spheres (Fig. 3),
whereas in P. patagonicus the groups appear
ther processing occurred, i.e. postfixation in
OSO (2%) and embedding in Araldite. Ultra- less compact. In general, the sperm of all three
4
species investigated are very simple, repre-
thin sections were cut with a Leica Ultracut.
senting a small (diameter approximately 2
Transmission electron microscopy was done
p.m) disc- or ovoid-shaped cell devoid of a
with Zeiss transmission electron microscopes.
flagellum (Figs. 3,'7, 8). The cell surface is
RESULTS
provided with conspicuous protuberances in
The male reproductive organs of E. mira- the ammotrechid species (Figs. 3, 7), there be-
bilis, O. gomezi and P. patagonicus are rather ing less obvious in E. mirabilis (Fig. 5, 8).
simple. They comprise a pair of tubular or- The electron-dense chromatin body (nuclear
gans starting from a common genital chamber. derivative) is relatively large. It is surrounded
—
Figures 3-6. Transmission electron micrographs. 3. Spherical sperm aggregate of Oltacola gomezi,
from vesicle. Note distinct protruberances of plasmalemmae of the sperm cells. Scale bar = |xm. 4.
1
Procleobis patagonicus, sperm cell from testis showing acrosomal complex. Scale bar = 0.5 pm. 5. Detail
of a sperm aggregate of Eusimonia mirabilis, from testis lumen. Note regular aiTangement of sperm cells.
Two discoid sperms form a pair with opposed acrosomal vacuoles. Scale bar — 0.5jam. 6. Sperm cells
from germ layer of testis of Cyta latirostris (Actinotrichida, Bdellidae). Scale bar = 0.5gm. Abbreviations:
AF = acrosomal filament, AV = acrosomal vacuole, M = mitochondrion, N = nucleus, PT = protuber-
ances, SE = secretion.
ALBERTI & PERETTI—MALE GENITAL SYSTEM AND SPERM IN SOLIFUGAE 271
IBM
i
272 THE JOURNAL OF ARACHNOLOGY
—
Figures 7—9, Line drawings of sperm cells. 7. Procleobis patagoniciis. 8. Eusimonia mirabilis, detail
of a logitiidinally sectioned sperm aggregate (from Alberti 1980a). 9. Bdellci septentrionalis (Actinotri-
chida, Bdellidae) in longitudinal section (from Alberti & Storch 1976). Scale bars = O.Spm, Abbreviations:
AF = acrosomal filament, AV = acrosomal vacuole, M = mitochondrion, N = nucleus, NC = nuclear
canal, NP = nuclear prolongation, PL = plasmalemma, PT = protuberances, SAM = subacrosomal
SSH =
material, secretion sheath.
by only a small amount of cytoplasm, con- berti (1980a). Hence it is now possible to
A
taining small mitochondria. small, flat ac- compare the sperm structure of Solifugae
rosomal vacuole is located close to the plas- more reliably with that of other arachnid taxa.
malemma (Figs. 4, 7). The vacuole is Earlier statements (Alberti 1980a, b, 1984,
underlain by subacrosomal material, from 1991, 1995, 2000) that the most similar sperm
which arises an acrosomal filament (jierfora- cells are found within the actinotrichid mites
torium) that penetrates the chromatin body are confirmed (Figs. 6, 9). Sperm cells of rep-
and finally encircles the chromatin body. resentatives of both taxa are small, devoid of
a flagellum, contain a chromatin body that is
DISCUSSION
penetrated and surrounded by circles of the
Our observations agree with the light mi- acrosomal filament, and have a tendency to
croscopic results obtained by Vachon (1945) form peripheral protuberances. Sperm cells of
and Junqua (1966) for species of Galeodidae. Anactinotrichida are profoundly different (Al-
Contrary to these authors, Roewer (1934), fol- berti 1980b, c, 1984, 1991, 2000; Alberti &
lowing Birula (1893-94), also illustrated a Coons 1999). Thus, sperm morphology re-
number of small accessory glands connected flects the remarkable differences that occur
to the genital chamber in Galeodes araneoides also between many other character states of
We
(Pallas 1772). have not yet studied this the both major groups of Acari and the ques-
area in our specimens. The fine structure of tion whether Acari represent a monophylum
the male system and spermatozoa of the am- or not has been discussed by several authors
motrechid species is in accordance with that (see Lindquist 1984; Hammen 1989; Evans
&
of the karschiid species investigated by Al- 1992; Alberti Coons 1999). Because of the
ALBERTI & PERETTI—MALE GENITAL SYSTEM AND SPERM IN SOLIFUGAE 273
general simplicity of solifugid and actinotri- Cordoba, Argentina. Both authors acknowl-
chid sperm cells, we cannot categorically dis- edge the suggestions of the referees and the
miss the possibility that these similarities are editor that helped to improve the manuscript.
the result of convergence. However, the sim-
LITERATURE CITED
ilarity in the fundamental organization of the
testis tissue seems to be noteworthy: in both Alberti, G. 1980a. Zur Feinstruktur des Hodenepi-
taxa there is a large glandular area that prob- thels und der Spermien von Eusimonia mirabilis
Roewer, 1934 (Solifugae, Arachnida). Zoolo-
ably produces secretions needed for spermato-
gischer Anzeiger 204:345-352.
phore formation. This has not been observed
Alberti, G. 1980b. Zur Feinstruktur der Spermien
in other arachnids (Alberti 1991, 1995, 2000).
und Spermiocytogenese der Milben (Acari): 1.
Sperm aggregates are also found in certain ac-
Anactinotrichida. Zoologische Jahrbiicher. Abtei-
tinotrichid mites, but may also occur in other lung ftir Anatomic und Ontogenie der Tiere 104:
&
arachnid groups (Alberti 1988; Peretti Bat- 77-138.
tan-Horenstein 2000). Evidently, a close re- Alberti, G. 1980c. Zur Feinstruktur der Spermien
lationship with Pseudoscorpiones, which have und Spermiocytogenese der Milben (Acari). II.
coiled-flagellate spermatozoa, is not supported Actinotrichida. Zoologische Jahrbiicher. Abtei-
by spermatological results. Except for the pe- lung fur Anatomic und Ontogenie der Tiere 104:
144-203.
culiar coiling of the flagellate spermatids at
Alberti, G. 1984. The contribution of comparative
the end of spermiogenesis, a process found
spermatology to problems of acarine systematics.
also in the Megoperculata (Uropygi, Ambly-
Pp. 479-490. In Acarology VI, I. Vlth Interna-
pygi, Araneae) and Ricinulei, the sperm cells
tional Congress of Acarology, Edinburgh. (D.A.
of Pseudoscorpiones are most similar to those Griffiths & C.E. Bowman, eds.). Ellis Norwood
of Scorpiones. Remarkably, the sperm cells of Press, Chichester.
both these latter taxa have strongly modified Alberti, G. 1988. Sperm Aggregations in Arachni-
mitochondria and retain a flagellar tunnel (Al- da. P. 331. In XL Europaisches Arachnologisches
berti 2000). If the similarities between Soli- Colloquium, Berlin 1988 (J. Haupt, ed.). TUB-
fugae and Actinotrichida pointed out here are Dokumentation 38, Berlin.
considered to be result of convergence, one Alberti, G. 1991. Spermatology in the Acari: Sys-
tematic and functional implications. Pp. 77-105.
needs to develop a hypothesis about selective
In The Acari: Reproduction, Development and
forces that could favor evolution of these
Life-History Strategies. 1st Symposium of the
characteristics. Remarkably, a simple correla-
European Association of Acarologists, Graz
tion between sperm morphology and sperm 1988 (R. Schuster & P.W. Murphy, eds.). Chap-
transfer, which might be expected, is not yet man & Hall, London.
evident (see Schaller 1979; Weygoldt 1990; Alberti, G. 1995. Comparative spermatology of
Alberti 2000). Alternatively, the assumption Chelicerata: Review and Perspective. Pp. 203-
of monophyly for Haplocnemata and Acari 230. In Advances in Spermatozoal Phylogeny
&
should be reconsidered. and Taxonomy. (B. G. M. Jamieson, J. Ausio
J.-L. Justine, eds.) Memoires du Museum Na-
ACKNOWLEDGMENTS
tional d’Histoire Naturelle. 166.
Alberti, G. 2000. Chelicerata. Pp. 31 1-388. In Pro-
The skillful assistance of G. Schittek in pre-
gress in Male Gamete Ultrastructure and Phylog-
paring the drawings is gratefully appreciated. eny. (B.G.M, Jamieson, ed.). In Reproductive Bi-
G.A. received financial support from the ology of the Invertebrates. (K.G. Adiyodi & R.G.
Deutsche Forschungsgemeinschaft (DEG; AL Adiyodi, eds.). Vol. 9B. Oxford & IBH Publish-
138/6). He also wishes to express his thanks ing/Wiley, New Delhi & N.Y.
—
&
to the Congress organizers for their kind hos- Alberti, G. L.B. Coons. 1999. Acari Mites. Pp.
pitality and to his acarological colleague, 515-1265. In Microscopic Anatomy of Inverte-
Shawnie Kramer, for her generous help to brates. (EW. Harrison, ed.). Vol. 8C. John Wiley
& New
reach the beautiful Congress site. A. V. P re- Sons, I&nc., York.
Alberti, G. V. Storch. 1976. Spermiocytogenese,
ceived financial support from the Consejo Na-
Spermien und Spermatophore von Schnabelmil-
cional de Investigaciones Cientificas y Tec-
ben (Bdellidae, Acari). Acta Zoologica (Stock-
nicas de Argentina (CONICET) and Provincia
holm) 57:177-188.
de Cordoba (CONICOR). He thanks Camilo Birula A. 1893-94. Untersuchungen iiber den Bau
1. Mattoni for his help with capturing solpug- der Geschlechtsorgane bei den Galeodiden. Biol-
ids during the trips to the Salinas Grandes, ogisches Centralblatt 11:295-300.
274 THE JOURNAL OF ARACHNOLOGY
Dunlop, J.A. 2000. The epistomo-labral plate and In Klassen und Ordnungen des Tierreichs. Vol.
lateral lips in solifuges, pseudoscorpions and 5, 4, 4 (H. G. Bronn, ed.). Akademische Ver-
mites. Ekologia (Bratislava) 19,Supplement 3: lagsgesellschaft, Leipzig.
67-78. Schaller, E 1979. Significance of sperm transfer and
Evans, G.O. 1992. Principles of Acarology. Wal- formation of spermatophores in arthropod phy-
lingford: C.A.B International. Pp 563. logeny. Pp. 587-608. In Arthropod Phylogeny.
Hammen, L. 1989. An Introduction to Comparative (A. P. Gupta, ed.). Van Nostrand Reinhold Com-
Arachnology. SPB Publishing bv. The Hague. pany, New York.
576pp. Shultz, J.W. 1990. Evolutionary morphology and
Jamieson, B.G.M. 1987. The Ultrastructure and phylogeny of Arachnida. Cladistics 6:1-38.
Phylogeny of Insect Spermatozoa. Cambridge Vachon, M. 1945. Sur les organes genitaux de qu-
University Press, Cambridge. 320pp. elques Solifuges (Arachnides). Bulletin du Mu-
Junqua, C. 1966. Recherches biologiques et histo- seum d’Histoire Naturelle (2) 17:—476-482.
physiologiques sur un Solifuge Saharien Othoes Weygoldt, P. 1990. Arthropoda Chelicerata:
saharae Panouse. Memoires du Museum Nation- Sperm transfer. Pp. 77-1 19. In Reproductive Bi-
al d’Histoire Naturelle, Series A, 43:1-124. ology of the Invertebrates. Vol. 4B. In Fertiliza-
Lindquist, E.E. 1984. Current theories on the evo- tion, Development, and Parental Care. (K.G.
lution of major groups of Acari and on their re- Adiyodi & R.G. Adiyodi, eds.). Oxford & IBH
PublishingAViley, New Delhi & N.Y
lationships with other groups of Arachnida, with
Weygoldt, P 1998. Evolution and systematics ofthe
consequent implications for their classification.
& Chelicerata. Experimental and Applied Acarolo-
Pp. 28-62. In Acarology VI. (D. A. Griffiths
C. E. Bowman, eds.). Vol. 1. Ellis Horwood, gy 22:63-7&9.
Weygoldt, P. H.E Paulus. 1979a. Untersuchungen
Chichester.
zur Morphologie, Taxonomie und Phylogenie der
Moritz, M. 1993. Unterstamm Arachnata. Pp. 64-
Chelicerata. Morphologische Untersuchungen.
442. In Lehrbuch der Speziellen Zoologie (begr. I.
Zeitschrift ftir Zoologische Systematik und Ev-
von A. Kaestner). 4.ed. Bd. Wirbellose Tiere.
1 : olutionsforschung 17:85-116.
4. Teil: Arthropoda. (H.-E. Gruner, ed.): G. Fi- &
Weygoldt, P. H.E Paulus. 1979b. Untersuchungen
scher Verlag, Jena.
zur Morphologie, Taxonomie und Phylogenie der
Peretti, A.V. & M. Battan-Horenstein. 2000. Mor-
Chelicerata. II. Cladogramme und die Entfaltung
phology of the male reproductive system in
der Chelicerata. Zeitschrift ftir zoologische Sys-
Buthidae and Bothriuridae species (Arachnida,
tematik und Evolutionsforschung 17:177-200.
Scorpiones). Abstract Book II, 23rd International Wheeler, WC. & C.Y. Hayashi. 1998. The phylog-
Congress of Entomology. Brazil:800. eny of the extant chelicerate orders. Cladistics
Punzo, E 1998. The Biology of Camel Spiders
14:173-192.
(Arachnida, Solifugae). Kluwer Academic Publ.,
Boston. 301pp. Manuscript received 1 July 2001, revised 28 No-
Roewer, C. Fr. 1934. Solifugae, Palpigradi. P. 723. vember 2001.