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Convergent Reduction of Ovariole Number Associated with Subterranean Life in Beetles.

Faille A, Pluot-Sigwalt D - PLoS ONE (2015)

Bottom Line: We discuss the multiple convergent evolutions in ovariole number and the potential link between a reduction of ovariole number and troglobiomorphism in a phylogenetic context.A reduction to one ovariole has occurred independently at least twice in this subterranean group.A reduction in the number of ovarioles in ground beetles is one of the striking consequences of subterranean specialization and it is correlated with another remarkable adaptation of subterranean beetles, a reduction in the number of larval instars.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Zoologische Staatssammlung, Munich, Germany.

ABSTRACT

Background: Some species of obligate cavernicolous beetles are known to possess a unique feature-a contraction of the larval cycle. In contrast to many other subterranean beetles, life-cycle contraction in Trechini ground beetles (Carabidae) is correlated with a reduction in the number of eggs and a drastic reduction in the number of ovarioles. This remarkable peculiarity has only been reported for a small number of closely related species.

Results: We give a description of the female internal reproductive system for six species of Trechini, including five subterranean species, with a particular focus on the western Pyrenean radiation of Aphaenops, a group for which nothing is known regarding the early life stages. We redescribe the internal female genitalia of A. crypticola Linder. Study of the ovarioles allowed us to infer the postembryonic development of the larvae for each species examined. We then used a phylogenetic framework to recognize two independent reductions in the number of ovarioles in the Pyrenean lineage. We discuss the multiple convergent evolutions in ovariole number and the potential link between a reduction of ovariole number and troglobiomorphism in a phylogenetic context.

Conclusions: There is an extreme reduction in ovariole number and size within the species studied; the eggs produced by small ovarioles have a remarkably large size. A reduction to one ovariole has occurred independently at least twice in this subterranean group. A reduction in the number of ovarioles in ground beetles is one of the striking consequences of subterranean specialization and it is correlated with another remarkable adaptation of subterranean beetles, a reduction in the number of larval instars.

No MeSH data available.


Related in: MedlinePlus

Female reproductive system and defense glands in five species of subterranean beetles of the tribe Trechini.Dorsal view, muscle fibers only shown on Fig 1E. (A) Trechus bordei. (B) Aphaenops loubensi. (C) Aphaenops ochsi ssp. cabidochei (apical acinous gland of defense glands not drawn). (D) Aphaenops leschenaulti (apical acinous gland of defense glands not drawn). (E) Aphaenops crypticola (paired defense glands not drawn). Scale bars: A = 5 mm; B, C, D = 1 mm; E = 0.5 mm. Abbreviations: cc = collecting canal of defense glands, dgl = defense gland, gd = genital duct surrounded by a muscular sheath, mf = muscle fibers, mt VIII = mediotergite VIII, oo = oocyte, ov = ovariole, pp = protruding part of genital duct, r = reservoir of defense glands, s = spermatheca, tf = terminal filament.
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pone.0131986.g001: Female reproductive system and defense glands in five species of subterranean beetles of the tribe Trechini.Dorsal view, muscle fibers only shown on Fig 1E. (A) Trechus bordei. (B) Aphaenops loubensi. (C) Aphaenops ochsi ssp. cabidochei (apical acinous gland of defense glands not drawn). (D) Aphaenops leschenaulti (apical acinous gland of defense glands not drawn). (E) Aphaenops crypticola (paired defense glands not drawn). Scale bars: A = 5 mm; B, C, D = 1 mm; E = 0.5 mm. Abbreviations: cc = collecting canal of defense glands, dgl = defense gland, gd = genital duct surrounded by a muscular sheath, mf = muscle fibers, mt VIII = mediotergite VIII, oo = oocyte, ov = ovariole, pp = protruding part of genital duct, r = reservoir of defense glands, s = spermatheca, tf = terminal filament.

Mentions: Trechus bordei possesses 5 to 7 polytrophic ovarioles per ovary (Fig 1A). The polytrophic type of ovariole is the rule within the entire group Adephaga. In polytrophic ovarioles, each follicle contains a number of trophocytes (nurse cells) together with one oocyte [35–37]. Ovarioles are tubular and elongate, attached together at the anterior end by their terminal filament. Germarium and vitellarium are distinct and the latter contains one or two small, immature basal oocytes. Pedicels are also elongated and seem to open directly into the median oviduct, the lateral oviducts being either extremely reduced or absent. The totality of the genital efferent system is enveloped in a thick layer of musculature (mainly circular muscle fibers, as illustrated in Fig 1E) to such an extent that the median oviduct, the vagina and the bursa copulatrix cannot be distinguished from each other. Between the ovaries there is a prominent median blind tube might be erroneously interpreted as a diverticulum of the genital efferent system, or a spermatheca or an accessory gland. However, treatment with KOH revealed that this tube is in fact the apical part of the bursa copulatrix tightly coated by a muscular sheath (see below). In one female specimen this tube-like projection was indistinct.


Convergent Reduction of Ovariole Number Associated with Subterranean Life in Beetles.

Faille A, Pluot-Sigwalt D - PLoS ONE (2015)

Female reproductive system and defense glands in five species of subterranean beetles of the tribe Trechini.Dorsal view, muscle fibers only shown on Fig 1E. (A) Trechus bordei. (B) Aphaenops loubensi. (C) Aphaenops ochsi ssp. cabidochei (apical acinous gland of defense glands not drawn). (D) Aphaenops leschenaulti (apical acinous gland of defense glands not drawn). (E) Aphaenops crypticola (paired defense glands not drawn). Scale bars: A = 5 mm; B, C, D = 1 mm; E = 0.5 mm. Abbreviations: cc = collecting canal of defense glands, dgl = defense gland, gd = genital duct surrounded by a muscular sheath, mf = muscle fibers, mt VIII = mediotergite VIII, oo = oocyte, ov = ovariole, pp = protruding part of genital duct, r = reservoir of defense glands, s = spermatheca, tf = terminal filament.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4494710&req=5

pone.0131986.g001: Female reproductive system and defense glands in five species of subterranean beetles of the tribe Trechini.Dorsal view, muscle fibers only shown on Fig 1E. (A) Trechus bordei. (B) Aphaenops loubensi. (C) Aphaenops ochsi ssp. cabidochei (apical acinous gland of defense glands not drawn). (D) Aphaenops leschenaulti (apical acinous gland of defense glands not drawn). (E) Aphaenops crypticola (paired defense glands not drawn). Scale bars: A = 5 mm; B, C, D = 1 mm; E = 0.5 mm. Abbreviations: cc = collecting canal of defense glands, dgl = defense gland, gd = genital duct surrounded by a muscular sheath, mf = muscle fibers, mt VIII = mediotergite VIII, oo = oocyte, ov = ovariole, pp = protruding part of genital duct, r = reservoir of defense glands, s = spermatheca, tf = terminal filament.
Mentions: Trechus bordei possesses 5 to 7 polytrophic ovarioles per ovary (Fig 1A). The polytrophic type of ovariole is the rule within the entire group Adephaga. In polytrophic ovarioles, each follicle contains a number of trophocytes (nurse cells) together with one oocyte [35–37]. Ovarioles are tubular and elongate, attached together at the anterior end by their terminal filament. Germarium and vitellarium are distinct and the latter contains one or two small, immature basal oocytes. Pedicels are also elongated and seem to open directly into the median oviduct, the lateral oviducts being either extremely reduced or absent. The totality of the genital efferent system is enveloped in a thick layer of musculature (mainly circular muscle fibers, as illustrated in Fig 1E) to such an extent that the median oviduct, the vagina and the bursa copulatrix cannot be distinguished from each other. Between the ovaries there is a prominent median blind tube might be erroneously interpreted as a diverticulum of the genital efferent system, or a spermatheca or an accessory gland. However, treatment with KOH revealed that this tube is in fact the apical part of the bursa copulatrix tightly coated by a muscular sheath (see below). In one female specimen this tube-like projection was indistinct.

Bottom Line: We discuss the multiple convergent evolutions in ovariole number and the potential link between a reduction of ovariole number and troglobiomorphism in a phylogenetic context.A reduction to one ovariole has occurred independently at least twice in this subterranean group.A reduction in the number of ovarioles in ground beetles is one of the striking consequences of subterranean specialization and it is correlated with another remarkable adaptation of subterranean beetles, a reduction in the number of larval instars.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Zoologische Staatssammlung, Munich, Germany.

ABSTRACT

Background: Some species of obligate cavernicolous beetles are known to possess a unique feature-a contraction of the larval cycle. In contrast to many other subterranean beetles, life-cycle contraction in Trechini ground beetles (Carabidae) is correlated with a reduction in the number of eggs and a drastic reduction in the number of ovarioles. This remarkable peculiarity has only been reported for a small number of closely related species.

Results: We give a description of the female internal reproductive system for six species of Trechini, including five subterranean species, with a particular focus on the western Pyrenean radiation of Aphaenops, a group for which nothing is known regarding the early life stages. We redescribe the internal female genitalia of A. crypticola Linder. Study of the ovarioles allowed us to infer the postembryonic development of the larvae for each species examined. We then used a phylogenetic framework to recognize two independent reductions in the number of ovarioles in the Pyrenean lineage. We discuss the multiple convergent evolutions in ovariole number and the potential link between a reduction of ovariole number and troglobiomorphism in a phylogenetic context.

Conclusions: There is an extreme reduction in ovariole number and size within the species studied; the eggs produced by small ovarioles have a remarkably large size. A reduction to one ovariole has occurred independently at least twice in this subterranean group. A reduction in the number of ovarioles in ground beetles is one of the striking consequences of subterranean specialization and it is correlated with another remarkable adaptation of subterranean beetles, a reduction in the number of larval instars.

No MeSH data available.


Related in: MedlinePlus