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Early embryonic determination of the sexual dimorphism in segment number in geophilomorph centipedes.

Brena C, Green J, Akam M - Evodevo (2013)

Bottom Line: Sexual dimorphism in segment number is not associated with terminal segment differentiation, but must instead be related to some earlier process during segment patterning.The dimorphism may be associated with a difference in the rate and/or duration of segment addition during the main phase of rapid segment addition that precedes embryonic Stage 6.This suggests that the adaptive role, if any, of the dimorphism is likely to be related to segment number per se, and not to sexual differentiation of the terminal region.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratory for Development and Evolution, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK. cb508@cam.ac.uk.

ABSTRACT

Background: Most geophilomorph centipedes show intraspecific variability in the number of leg-bearing segments. This intraspecific variability generally has a component that is related to sex, with females having on average more segments than males. Neither the developmental basis nor the adaptive role of this dimorphism is known.

Results: To determine when this sexual dimorphism in segment number is established, we have followed the development of Strigamia maritima embryos from the onset of segmentation to the first post-embryonic stage where we could determine the sex morphologically. We find that males and females differ in segment number by Stage 6.1, a point during embryogenesis when segment addition pauses while the embryo undergoes large-scale movements. We have confirmed this pattern by establishing a molecular method to determine the sex of single embryos, utilising duplex PCR amplification for Y chromosomal and autosomal sequences. This confirms that male embryos have a modal number of 43 segments visible at Stage 6, while females have 45. In our Strigamia population, adult males have a modal number of 47 leg-bearing segments, and females have 49. This implies that the sexual dimorphism in segment number is determined before the addition of the last leg-bearing segments and the terminal genital segments.

Conclusions: Sexual dimorphism in segment number is not associated with terminal segment differentiation, but must instead be related to some earlier process during segment patterning. The dimorphism may be associated with a difference in the rate and/or duration of segment addition during the main phase of rapid segment addition that precedes embryonic Stage 6. This suggests that the adaptive role, if any, of the dimorphism is likely to be related to segment number per se, and not to sexual differentiation of the terminal region.

No MeSH data available.


Related in: MedlinePlus

Strigamia embryonic and post-embryonic stages used for leg-bearing segment counting and sex determination. (A) Lateral view of an early Stage 6 embryo, live in mineral oil: lateral illumination and black background allow segment counting (45 leg-bearing segments (LBSs) in this specimen, see insert). (B) An early Stage 6 flat-mounted germ band, stained with DAPI (4′,6-diamidino-2-phenylindole) to highlight the morphology. The stage of this specimen corresponds to that of the embryo shown in (A) and is characterised by the lateral spreading of the germ band in its middle portion. This specimen has 43 LBSs; the 44th LBS here begins to appear, but would not be visible in the live embryo. (C), (D), (E) Adolescens I stage: (C) live specimen in mineral oil, lateral view; (D), (E) high magnification of the ventral side of the terminal trunk mounted on a slide and viewed at the compound microscope with Nomarski optics. This is the first stage at which it is possible to determine the sex because of the sexual differentiation of the genital sternite (arrowhead), with lateral protrusions in males (D) and rounded in females (E). At this stage, the legs of the last LBS are already distinct, notably by the swollen coxopleuron, but they are not obviously different in males and females. (F), (G) Final differentiation between live adult male and female: in the studied population, the modal number of LBSs in males is 47 (F) and in females is 49 (G). By this stage the last pair of legs are highly modified in the male, swollen and bearing sensory and glandular structures (F,F1). (F), (G) dorsal view; (F1), (G1) ventral magnified view of, respectively, (F) and (G). a, antenna; p, proctodeum.*Artefactual rupture of the germ band. Scale bar: (A), (B) 300 μm; (C) 1mm; (D), (E) 100 μm; (F), (G) 1 mm; (F1), (G1) 300 μm.
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Figure 1: Strigamia embryonic and post-embryonic stages used for leg-bearing segment counting and sex determination. (A) Lateral view of an early Stage 6 embryo, live in mineral oil: lateral illumination and black background allow segment counting (45 leg-bearing segments (LBSs) in this specimen, see insert). (B) An early Stage 6 flat-mounted germ band, stained with DAPI (4′,6-diamidino-2-phenylindole) to highlight the morphology. The stage of this specimen corresponds to that of the embryo shown in (A) and is characterised by the lateral spreading of the germ band in its middle portion. This specimen has 43 LBSs; the 44th LBS here begins to appear, but would not be visible in the live embryo. (C), (D), (E) Adolescens I stage: (C) live specimen in mineral oil, lateral view; (D), (E) high magnification of the ventral side of the terminal trunk mounted on a slide and viewed at the compound microscope with Nomarski optics. This is the first stage at which it is possible to determine the sex because of the sexual differentiation of the genital sternite (arrowhead), with lateral protrusions in males (D) and rounded in females (E). At this stage, the legs of the last LBS are already distinct, notably by the swollen coxopleuron, but they are not obviously different in males and females. (F), (G) Final differentiation between live adult male and female: in the studied population, the modal number of LBSs in males is 47 (F) and in females is 49 (G). By this stage the last pair of legs are highly modified in the male, swollen and bearing sensory and glandular structures (F,F1). (F), (G) dorsal view; (F1), (G1) ventral magnified view of, respectively, (F) and (G). a, antenna; p, proctodeum.*Artefactual rupture of the germ band. Scale bar: (A), (B) 300 μm; (C) 1mm; (D), (E) 100 μm; (F), (G) 1 mm; (F1), (G1) 300 μm.

Mentions: We can consider two general models for the developmental origin of this sexual dimorphism in segment number. One model, which we initially considered the most likely, focuses on the fact that the genital segments of centipedes lie at the extreme posterior end of the body. The last pair of leg-bearing segments is strikingly dimorphic in many species (see, for example, Figure 1F,G), and behind this there are highly modified segments associated with the gonopods, gonopores and egg-laying apparatus. Little is known about the development of these genital segments, which are not developed at hatching. It seemed possible that different numbers of segments may be specified according to sex in this extreme posterior region, or that segment primordia might develop differentially in the two sexes, such that two segments which in females develop as leg-bearing segments might make no appendages, or specialised genital structures, in males. Something similar is known to happen in Drosophila and some other Diptera, where male and female external genitalia develop from different segmental primordia [9,10].


Early embryonic determination of the sexual dimorphism in segment number in geophilomorph centipedes.

Brena C, Green J, Akam M - Evodevo (2013)

Strigamia embryonic and post-embryonic stages used for leg-bearing segment counting and sex determination. (A) Lateral view of an early Stage 6 embryo, live in mineral oil: lateral illumination and black background allow segment counting (45 leg-bearing segments (LBSs) in this specimen, see insert). (B) An early Stage 6 flat-mounted germ band, stained with DAPI (4′,6-diamidino-2-phenylindole) to highlight the morphology. The stage of this specimen corresponds to that of the embryo shown in (A) and is characterised by the lateral spreading of the germ band in its middle portion. This specimen has 43 LBSs; the 44th LBS here begins to appear, but would not be visible in the live embryo. (C), (D), (E) Adolescens I stage: (C) live specimen in mineral oil, lateral view; (D), (E) high magnification of the ventral side of the terminal trunk mounted on a slide and viewed at the compound microscope with Nomarski optics. This is the first stage at which it is possible to determine the sex because of the sexual differentiation of the genital sternite (arrowhead), with lateral protrusions in males (D) and rounded in females (E). At this stage, the legs of the last LBS are already distinct, notably by the swollen coxopleuron, but they are not obviously different in males and females. (F), (G) Final differentiation between live adult male and female: in the studied population, the modal number of LBSs in males is 47 (F) and in females is 49 (G). By this stage the last pair of legs are highly modified in the male, swollen and bearing sensory and glandular structures (F,F1). (F), (G) dorsal view; (F1), (G1) ventral magnified view of, respectively, (F) and (G). a, antenna; p, proctodeum.*Artefactual rupture of the germ band. Scale bar: (A), (B) 300 μm; (C) 1mm; (D), (E) 100 μm; (F), (G) 1 mm; (F1), (G1) 300 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
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Figure 1: Strigamia embryonic and post-embryonic stages used for leg-bearing segment counting and sex determination. (A) Lateral view of an early Stage 6 embryo, live in mineral oil: lateral illumination and black background allow segment counting (45 leg-bearing segments (LBSs) in this specimen, see insert). (B) An early Stage 6 flat-mounted germ band, stained with DAPI (4′,6-diamidino-2-phenylindole) to highlight the morphology. The stage of this specimen corresponds to that of the embryo shown in (A) and is characterised by the lateral spreading of the germ band in its middle portion. This specimen has 43 LBSs; the 44th LBS here begins to appear, but would not be visible in the live embryo. (C), (D), (E) Adolescens I stage: (C) live specimen in mineral oil, lateral view; (D), (E) high magnification of the ventral side of the terminal trunk mounted on a slide and viewed at the compound microscope with Nomarski optics. This is the first stage at which it is possible to determine the sex because of the sexual differentiation of the genital sternite (arrowhead), with lateral protrusions in males (D) and rounded in females (E). At this stage, the legs of the last LBS are already distinct, notably by the swollen coxopleuron, but they are not obviously different in males and females. (F), (G) Final differentiation between live adult male and female: in the studied population, the modal number of LBSs in males is 47 (F) and in females is 49 (G). By this stage the last pair of legs are highly modified in the male, swollen and bearing sensory and glandular structures (F,F1). (F), (G) dorsal view; (F1), (G1) ventral magnified view of, respectively, (F) and (G). a, antenna; p, proctodeum.*Artefactual rupture of the germ band. Scale bar: (A), (B) 300 μm; (C) 1mm; (D), (E) 100 μm; (F), (G) 1 mm; (F1), (G1) 300 μm.
Mentions: We can consider two general models for the developmental origin of this sexual dimorphism in segment number. One model, which we initially considered the most likely, focuses on the fact that the genital segments of centipedes lie at the extreme posterior end of the body. The last pair of leg-bearing segments is strikingly dimorphic in many species (see, for example, Figure 1F,G), and behind this there are highly modified segments associated with the gonopods, gonopores and egg-laying apparatus. Little is known about the development of these genital segments, which are not developed at hatching. It seemed possible that different numbers of segments may be specified according to sex in this extreme posterior region, or that segment primordia might develop differentially in the two sexes, such that two segments which in females develop as leg-bearing segments might make no appendages, or specialised genital structures, in males. Something similar is known to happen in Drosophila and some other Diptera, where male and female external genitalia develop from different segmental primordia [9,10].

Bottom Line: Sexual dimorphism in segment number is not associated with terminal segment differentiation, but must instead be related to some earlier process during segment patterning.The dimorphism may be associated with a difference in the rate and/or duration of segment addition during the main phase of rapid segment addition that precedes embryonic Stage 6.This suggests that the adaptive role, if any, of the dimorphism is likely to be related to segment number per se, and not to sexual differentiation of the terminal region.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratory for Development and Evolution, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK. cb508@cam.ac.uk.

ABSTRACT

Background: Most geophilomorph centipedes show intraspecific variability in the number of leg-bearing segments. This intraspecific variability generally has a component that is related to sex, with females having on average more segments than males. Neither the developmental basis nor the adaptive role of this dimorphism is known.

Results: To determine when this sexual dimorphism in segment number is established, we have followed the development of Strigamia maritima embryos from the onset of segmentation to the first post-embryonic stage where we could determine the sex morphologically. We find that males and females differ in segment number by Stage 6.1, a point during embryogenesis when segment addition pauses while the embryo undergoes large-scale movements. We have confirmed this pattern by establishing a molecular method to determine the sex of single embryos, utilising duplex PCR amplification for Y chromosomal and autosomal sequences. This confirms that male embryos have a modal number of 43 segments visible at Stage 6, while females have 45. In our Strigamia population, adult males have a modal number of 47 leg-bearing segments, and females have 49. This implies that the sexual dimorphism in segment number is determined before the addition of the last leg-bearing segments and the terminal genital segments.

Conclusions: Sexual dimorphism in segment number is not associated with terminal segment differentiation, but must instead be related to some earlier process during segment patterning. The dimorphism may be associated with a difference in the rate and/or duration of segment addition during the main phase of rapid segment addition that precedes embryonic Stage 6. This suggests that the adaptive role, if any, of the dimorphism is likely to be related to segment number per se, and not to sexual differentiation of the terminal region.

No MeSH data available.


Related in: MedlinePlus