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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

Number of ovarioles mapped on simplified phylogram of Trechini.Simplified phylogram of Trechini obtained with RAxML using a combined data matrix of mitochondrial (cox1, rrnL+trnL and nad1) and nuclear (LSU, SSU) markers. Troglobitic species marked with a “T” in a black circle. *: bootstrap >95. The number of ovarioles per ovary is indicated after the species name. Colors indicate number of ovarioles: red: 1, blue: 2, orange: 3, violet: 3–4, green: 5, black: >5.
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pone.0131986.g004: Number of ovarioles mapped on simplified phylogram of Trechini.Simplified phylogram of Trechini obtained with RAxML using a combined data matrix of mitochondrial (cox1, rrnL+trnL and nad1) and nuclear (LSU, SSU) markers. Troglobitic species marked with a “T” in a black circle. *: bootstrap >95. The number of ovarioles per ovary is indicated after the species name. Colors indicate number of ovarioles: red: 1, blue: 2, orange: 3, violet: 3–4, green: 5, black: >5.

Mentions: All the species of Aphaenops studied to date share the state of an ovary with a single ovariole. The genus Aphaenops is not monophyletic, and is represented by two independent subterranean radiations in the Pyrenees, one in the Eastern part (Cerbaphaenops), one in the Western part of the range (Aphaenops s. str.) [25]. Hydraphaenops, which is not monophyletic, was recently considered as a subgenus of Aphaenops, together with a new subgenus, Simaphaenops [26]. Most of the species belonging to these two groups are known by very few specimens, and the only species for which the number of ovarioles is known is A. (Hydraphaenops) ehlersi [15,19]. It has two ovarioles per ovary and an active larva ([19]; Table 1). Because A. (H.) ehlersi is phylogenetically closer to Cerbaphaenops than to the western Aphaenops s. str., the presence of more than one ovariole per ovary in this species indicates an independent reduction within the Pyrenean lineage of subterranean Trechini (Fig 4). The reduction to one ovariole has therefore occurred at least twice in Aphaenops. Other evidence that such a reduction occurred twice in the Pyrenean lineage is the presence of at least two ovarioles in the species of Geotrechus studied. Because the genus Geotrechus is not monophyletic [25], the regression in ovariole number in the two cave-adapted lineages of Trechini (eastern and western radiations) suggests an independent regressive evolution in the Pyrenean lineage. Unlike the Pyrenean species, the number of ovarioles is high in the Adriatic subterranean species Typhlotrechus bilimeki Sturm ([19]; Table 1). Typhlotrechus originated in the Oligocene and underwent little diversification (two species only) [21,24].


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

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

Number of ovarioles mapped on simplified phylogram of Trechini.Simplified phylogram of Trechini obtained with RAxML using a combined data matrix of mitochondrial (cox1, rrnL+trnL and nad1) and nuclear (LSU, SSU) markers. Troglobitic species marked with a “T” in a black circle. *: bootstrap >95. The number of ovarioles per ovary is indicated after the species name. Colors indicate number of ovarioles: red: 1, blue: 2, orange: 3, violet: 3–4, green: 5, black: >5.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0131986.g004: Number of ovarioles mapped on simplified phylogram of Trechini.Simplified phylogram of Trechini obtained with RAxML using a combined data matrix of mitochondrial (cox1, rrnL+trnL and nad1) and nuclear (LSU, SSU) markers. Troglobitic species marked with a “T” in a black circle. *: bootstrap >95. The number of ovarioles per ovary is indicated after the species name. Colors indicate number of ovarioles: red: 1, blue: 2, orange: 3, violet: 3–4, green: 5, black: >5.
Mentions: All the species of Aphaenops studied to date share the state of an ovary with a single ovariole. The genus Aphaenops is not monophyletic, and is represented by two independent subterranean radiations in the Pyrenees, one in the Eastern part (Cerbaphaenops), one in the Western part of the range (Aphaenops s. str.) [25]. Hydraphaenops, which is not monophyletic, was recently considered as a subgenus of Aphaenops, together with a new subgenus, Simaphaenops [26]. Most of the species belonging to these two groups are known by very few specimens, and the only species for which the number of ovarioles is known is A. (Hydraphaenops) ehlersi [15,19]. It has two ovarioles per ovary and an active larva ([19]; Table 1). Because A. (H.) ehlersi is phylogenetically closer to Cerbaphaenops than to the western Aphaenops s. str., the presence of more than one ovariole per ovary in this species indicates an independent reduction within the Pyrenean lineage of subterranean Trechini (Fig 4). The reduction to one ovariole has therefore occurred at least twice in Aphaenops. Other evidence that such a reduction occurred twice in the Pyrenean lineage is the presence of at least two ovarioles in the species of Geotrechus studied. Because the genus Geotrechus is not monophyletic [25], the regression in ovariole number in the two cave-adapted lineages of Trechini (eastern and western radiations) suggests an independent regressive evolution in the Pyrenean lineage. Unlike the Pyrenean species, the number of ovarioles is high in the Adriatic subterranean species Typhlotrechus bilimeki Sturm ([19]; Table 1). Typhlotrechus originated in the Oligocene and underwent little diversification (two species only) [21,24].

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