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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.


Rate of addition of leg-bearing segments through embryonic development. (A) Plots show the segment number each day for single embryos (each represented by a different colour) (n = 22); interrupted or fragmentary lines correspond to embryos for which sure daily data were not available. (B) Plots show the daily averaged segment number for the embryos of (A) having a leg-bearing segment (LBS) number value of 41 to 43 at Stage 6.1 (blue line, ‘mean st 6.1 43 LBS’) (n =14) and for the embryos of (A) having a LBS number value of 44 to 45 (red line, ‘mean st 6.1 45 LBS’) (n =8). (C) Plot comparing the red line of (B) (‘mean st 6.1 45 LBS’) with a selection (n =9) of those embryos whose sex has been determined at stage adolescens I. The plot shows that the trend of the daily mean values of (B) is a precise representation of the trend of known female individuals, with an adult LBS number of 49. LBS values at Stage 6.1 are marked by an arrow in (A) and are in yellow in (B) and (C) (specific values indicated in (B)). Negative LBS values indicate anterior, nonleg-bearing segments: 2, first maxilla segment; –1, second maxilla segment; 0, maxilliped segment.
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Figure 5: Rate of addition of leg-bearing segments through embryonic development. (A) Plots show the segment number each day for single embryos (each represented by a different colour) (n = 22); interrupted or fragmentary lines correspond to embryos for which sure daily data were not available. (B) Plots show the daily averaged segment number for the embryos of (A) having a leg-bearing segment (LBS) number value of 41 to 43 at Stage 6.1 (blue line, ‘mean st 6.1 43 LBS’) (n =14) and for the embryos of (A) having a LBS number value of 44 to 45 (red line, ‘mean st 6.1 45 LBS’) (n =8). (C) Plot comparing the red line of (B) (‘mean st 6.1 45 LBS’) with a selection (n =9) of those embryos whose sex has been determined at stage adolescens I. The plot shows that the trend of the daily mean values of (B) is a precise representation of the trend of known female individuals, with an adult LBS number of 49. LBS values at Stage 6.1 are marked by an arrow in (A) and are in yellow in (B) and (C) (specific values indicated in (B)). Negative LBS values indicate anterior, nonleg-bearing segments: 2, first maxilla segment; –1, second maxilla segment; 0, maxilliped segment.

Mentions: In the long-term culture experiment, the available data for animals that survived to adolescens I suggest that embryos scored as having 42 or 43 segments at Stage 6.1 are likely to be males, while embryos scored with 44 or 45 segments at this stage are likely to be females. If we use this criterion to assign sex, regardless of whether the individual survived long enough to be sexed, we can plot the trajectory of segment addition by sex, averaged on a daily basis for all individuals in the dataset (Figure 5B). This plot shows that putative males and females appear to differ slightly in the rate of segment addition during the rapid phase of trunk segment addition (Stage 4), but that from Stage 6 onwards the segment numbers of males and females at the same age maintain a constant difference of about two in segment number. If the data are averaged only for those females for which sex is definitively known, the plot is virtually identical to that for putative females in the entire dataset (Figure 5C). For males, too few sexed individuals are available to make this comparison meaningful.


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

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

Rate of addition of leg-bearing segments through embryonic development. (A) Plots show the segment number each day for single embryos (each represented by a different colour) (n = 22); interrupted or fragmentary lines correspond to embryos for which sure daily data were not available. (B) Plots show the daily averaged segment number for the embryos of (A) having a leg-bearing segment (LBS) number value of 41 to 43 at Stage 6.1 (blue line, ‘mean st 6.1 43 LBS’) (n =14) and for the embryos of (A) having a LBS number value of 44 to 45 (red line, ‘mean st 6.1 45 LBS’) (n =8). (C) Plot comparing the red line of (B) (‘mean st 6.1 45 LBS’) with a selection (n =9) of those embryos whose sex has been determined at stage adolescens I. The plot shows that the trend of the daily mean values of (B) is a precise representation of the trend of known female individuals, with an adult LBS number of 49. LBS values at Stage 6.1 are marked by an arrow in (A) and are in yellow in (B) and (C) (specific values indicated in (B)). Negative LBS values indicate anterior, nonleg-bearing segments: 2, first maxilla segment; –1, second maxilla segment; 0, maxilliped segment.
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Figure 5: Rate of addition of leg-bearing segments through embryonic development. (A) Plots show the segment number each day for single embryos (each represented by a different colour) (n = 22); interrupted or fragmentary lines correspond to embryos for which sure daily data were not available. (B) Plots show the daily averaged segment number for the embryos of (A) having a leg-bearing segment (LBS) number value of 41 to 43 at Stage 6.1 (blue line, ‘mean st 6.1 43 LBS’) (n =14) and for the embryos of (A) having a LBS number value of 44 to 45 (red line, ‘mean st 6.1 45 LBS’) (n =8). (C) Plot comparing the red line of (B) (‘mean st 6.1 45 LBS’) with a selection (n =9) of those embryos whose sex has been determined at stage adolescens I. The plot shows that the trend of the daily mean values of (B) is a precise representation of the trend of known female individuals, with an adult LBS number of 49. LBS values at Stage 6.1 are marked by an arrow in (A) and are in yellow in (B) and (C) (specific values indicated in (B)). Negative LBS values indicate anterior, nonleg-bearing segments: 2, first maxilla segment; –1, second maxilla segment; 0, maxilliped segment.
Mentions: In the long-term culture experiment, the available data for animals that survived to adolescens I suggest that embryos scored as having 42 or 43 segments at Stage 6.1 are likely to be males, while embryos scored with 44 or 45 segments at this stage are likely to be females. If we use this criterion to assign sex, regardless of whether the individual survived long enough to be sexed, we can plot the trajectory of segment addition by sex, averaged on a daily basis for all individuals in the dataset (Figure 5B). This plot shows that putative males and females appear to differ slightly in the rate of segment addition during the rapid phase of trunk segment addition (Stage 4), but that from Stage 6 onwards the segment numbers of males and females at the same age maintain a constant difference of about two in segment number. If the data are averaged only for those females for which sex is definitively known, the plot is virtually identical to that for putative females in the entire dataset (Figure 5C). For males, too few sexed individuals are available to make this comparison meaningful.

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.