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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

Aphaenops crypticola, oocyte.A gravid female with a mature oocyte in the right ovariole and the same oocyte in place within the female abdomen. Scale bar: 1 mm.
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pone.0131986.g002: Aphaenops crypticola, oocyte.A gravid female with a mature oocyte in the right ovariole and the same oocyte in place within the female abdomen. Scale bar: 1 mm.

Mentions: Aphaenops loubensi (Fig 1B), A. ochsi (Fig 1C), A. leschenaulti (Fig 1D) and A. crypticola (Fig 1E) possess only a single polytrophic ovariole per ovary. These single-ovariole ovaries are very small, somewhat sac-shaped, and usually embedded within a thick layer of fat body; the terminal filament is indistinct. The germarium and vitellarium are not distinct from each other, the pedicel is almost non-existent and lateral oviducts are probably absent. The other parts of the efferent genital duct—median oviduct, bursa copulatrix and vagina—are entirely enveloped in a dense, common sheath of musculature, such that they cannot be distinguished from one another. However, in A. crypticola (Fig 1E) a tube-like protrusion and a small pigmented vesicle project out of the thick muscle sheath; these structures were interpreted as forming the spermatheca (see below). One female of A. crypticola was gravid (Fig 2); the dextral ovariole contained a single, conspicuous, mature egg, with numerous, large, lipid-like spherules. As shown in Fig 2, the 2.1 mm long egg occupied most of the abdominal cavity, representing nearly half the length of the female (4.5mm). In contrast, the left ovariole appeared minute, containing only a small basal oocyte. The two ovarioles may function alternately.


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

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

Aphaenops crypticola, oocyte.A gravid female with a mature oocyte in the right ovariole and the same oocyte in place within the female abdomen. Scale bar: 1 mm.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0131986.g002: Aphaenops crypticola, oocyte.A gravid female with a mature oocyte in the right ovariole and the same oocyte in place within the female abdomen. Scale bar: 1 mm.
Mentions: Aphaenops loubensi (Fig 1B), A. ochsi (Fig 1C), A. leschenaulti (Fig 1D) and A. crypticola (Fig 1E) possess only a single polytrophic ovariole per ovary. These single-ovariole ovaries are very small, somewhat sac-shaped, and usually embedded within a thick layer of fat body; the terminal filament is indistinct. The germarium and vitellarium are not distinct from each other, the pedicel is almost non-existent and lateral oviducts are probably absent. The other parts of the efferent genital duct—median oviduct, bursa copulatrix and vagina—are entirely enveloped in a dense, common sheath of musculature, such that they cannot be distinguished from one another. However, in A. crypticola (Fig 1E) a tube-like protrusion and a small pigmented vesicle project out of the thick muscle sheath; these structures were interpreted as forming the spermatheca (see below). One female of A. crypticola was gravid (Fig 2); the dextral ovariole contained a single, conspicuous, mature egg, with numerous, large, lipid-like spherules. As shown in Fig 2, the 2.1 mm long egg occupied most of the abdominal cavity, representing nearly half the length of the female (4.5mm). In contrast, the left ovariole appeared minute, containing only a small basal oocyte. The two ovarioles may function alternately.

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