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Pupal remodeling and the evolution and development of alternative male morphologies in horned beetles.

Moczek AP - BMC Evol. Biol. (2007)

Bottom Line: Prepupal growth is not the only determinant of differences in male horn expression.This study is the first to document that male dimorphism in horned beetles is the product of two developmentaly dissociated processes: prepupal growth and pupal remodeling.More generally, adult morphology alone appears to provide few clues, if any, as to the relative contributions of both processes to the expression of alternative male morphs, underscoring the importance of developmental studies in efforts aimed at understanding the evolution of adult diversity patterns.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, Indiana University, Bloomington IN, USA. armin@indiana.edu.

ABSTRACT

Background: How novel morphological traits originate and diversify represents a major frontier in evolutionary biology. Horned beetles are emerging as an increasingly popular model system to explore the genetic, developmental, and ecological mechanisms, as well as the interplay between them, in the genesis of novelty and diversity. The horns of beetles originate during a rapid growth phase during the prepupal stage of larval development. Differential growth during this period is either implicitly or explicitly assumed to be the sole mechanism underlying differences in horn expression within and between species. Here I focus on male horn dimorphisms, a phenomenon at the center of many studies in behavioral ecology and evolutionary development, and quantify the relative contributions of a previously ignored developmental process, pupal remodeling, to the expression of male dimorphism in three horned beetle species.

Results: Prepupal growth is not the only determinant of differences in male horn expression. Instead, following their initial prepupal growth phase, beetles may be extensively remodeled during the subsequent pupal stage in a sex and size-dependent manner. Specifically, male dimorphism in the three Onthophagus species studied here was shaped not at all, partly or entirely by such pupal remodeling rather than differential growth, suggesting that pupal remodeling is phylogenetically widespread, evolutionarily labile, and developmentally flexible.

Conclusion: This study is the first to document that male dimorphism in horned beetles is the product of two developmentaly dissociated processes: prepupal growth and pupal remodeling. More generally, adult morphology alone appears to provide few clues, if any, as to the relative contributions of both processes to the expression of alternative male morphs, underscoring the importance of developmental studies in efforts aimed at understanding the evolution of adult diversity patterns.

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Ontogenetic changes in allometric scaling between body size and thoracic horn length in male Onthophagus nigriventris. (A) Scaling relationship between body size (presented as standard deviations away from mean) and horn length in male pupae (●) and corresponding adults (○). Allometries differ significantly both in amplitude and slope. (B) Absolute (■ right) and relative (□ left) loss of pupal horn length as a function of adult male body size. Both absolute and relative horn loss decline drastically with adult size.(C) Log-log plot of pupal against adult horn length. Gray line indicates expectation if adult horn length is a direct reflection of pupal horn length (y-intercept = 0, slope = 1). Regression analysis shows that the y-intercept is significantly different from 0 (indicating pupal remodeling) and the slope is significantly greater than 1 (indicating that remodeling occurs to a greater degree in minor compared to major male morphs). Red lines indicate 99% confidence intervals.
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Figure 2: Ontogenetic changes in allometric scaling between body size and thoracic horn length in male Onthophagus nigriventris. (A) Scaling relationship between body size (presented as standard deviations away from mean) and horn length in male pupae (●) and corresponding adults (○). Allometries differ significantly both in amplitude and slope. (B) Absolute (■ right) and relative (□ left) loss of pupal horn length as a function of adult male body size. Both absolute and relative horn loss decline drastically with adult size.(C) Log-log plot of pupal against adult horn length. Gray line indicates expectation if adult horn length is a direct reflection of pupal horn length (y-intercept = 0, slope = 1). Regression analysis shows that the y-intercept is significantly different from 0 (indicating pupal remodeling) and the slope is significantly greater than 1 (indicating that remodeling occurs to a greater degree in minor compared to major male morphs). Red lines indicate 99% confidence intervals.

Mentions: In O. nigriventris, scaling relationships between body size and horn length changed significantly from the pupal to the adult stage (Fig. 2A). Specifically, both amplitude and steepness of the slope increased significantly from the pupal to the adult stage, creating a greater and more sudden disparity between minor and major male morphs (amplitude: T64 = 2.76, p = 0.0075; slope: T64 = 2.53, p = 0.0139). Both relative and absolute loss of horn length decreased quickly with male size (Fig. 2B, Frel = 127; p < 0.0001; Fabs = 42; p < 0.0001). Small males commonly lost >1 mm (> 20%) of horn length compared to ~0.25 mm (< 5%) in large males. Log-log plots of pupal against adult horn length showed that hornless, minor males fell below the line expected if adult horn length was a direct, unaltered reflection of pupal horn length (indicated by gray line in Fig. 2C), whereas horned, major males appeared right on that line. This observation was backed up by regression analysis, which yielded a negative y-intercept significantly different from 0 (T32 = 18.95, p < 0.0001), confirming that horn lengths of at least some males decreased from the pupal to the adult stage, and with a slope highly significantly greater than 1 (Fig. 2C; T32 = 14.63; p < 0.0001), supporting that this decrease was strongest for small males.


Pupal remodeling and the evolution and development of alternative male morphologies in horned beetles.

Moczek AP - BMC Evol. Biol. (2007)

Ontogenetic changes in allometric scaling between body size and thoracic horn length in male Onthophagus nigriventris. (A) Scaling relationship between body size (presented as standard deviations away from mean) and horn length in male pupae (●) and corresponding adults (○). Allometries differ significantly both in amplitude and slope. (B) Absolute (■ right) and relative (□ left) loss of pupal horn length as a function of adult male body size. Both absolute and relative horn loss decline drastically with adult size.(C) Log-log plot of pupal against adult horn length. Gray line indicates expectation if adult horn length is a direct reflection of pupal horn length (y-intercept = 0, slope = 1). Regression analysis shows that the y-intercept is significantly different from 0 (indicating pupal remodeling) and the slope is significantly greater than 1 (indicating that remodeling occurs to a greater degree in minor compared to major male morphs). Red lines indicate 99% confidence intervals.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2117020&req=5

Figure 2: Ontogenetic changes in allometric scaling between body size and thoracic horn length in male Onthophagus nigriventris. (A) Scaling relationship between body size (presented as standard deviations away from mean) and horn length in male pupae (●) and corresponding adults (○). Allometries differ significantly both in amplitude and slope. (B) Absolute (■ right) and relative (□ left) loss of pupal horn length as a function of adult male body size. Both absolute and relative horn loss decline drastically with adult size.(C) Log-log plot of pupal against adult horn length. Gray line indicates expectation if adult horn length is a direct reflection of pupal horn length (y-intercept = 0, slope = 1). Regression analysis shows that the y-intercept is significantly different from 0 (indicating pupal remodeling) and the slope is significantly greater than 1 (indicating that remodeling occurs to a greater degree in minor compared to major male morphs). Red lines indicate 99% confidence intervals.
Mentions: In O. nigriventris, scaling relationships between body size and horn length changed significantly from the pupal to the adult stage (Fig. 2A). Specifically, both amplitude and steepness of the slope increased significantly from the pupal to the adult stage, creating a greater and more sudden disparity between minor and major male morphs (amplitude: T64 = 2.76, p = 0.0075; slope: T64 = 2.53, p = 0.0139). Both relative and absolute loss of horn length decreased quickly with male size (Fig. 2B, Frel = 127; p < 0.0001; Fabs = 42; p < 0.0001). Small males commonly lost >1 mm (> 20%) of horn length compared to ~0.25 mm (< 5%) in large males. Log-log plots of pupal against adult horn length showed that hornless, minor males fell below the line expected if adult horn length was a direct, unaltered reflection of pupal horn length (indicated by gray line in Fig. 2C), whereas horned, major males appeared right on that line. This observation was backed up by regression analysis, which yielded a negative y-intercept significantly different from 0 (T32 = 18.95, p < 0.0001), confirming that horn lengths of at least some males decreased from the pupal to the adult stage, and with a slope highly significantly greater than 1 (Fig. 2C; T32 = 14.63; p < 0.0001), supporting that this decrease was strongest for small males.

Bottom Line: Prepupal growth is not the only determinant of differences in male horn expression.This study is the first to document that male dimorphism in horned beetles is the product of two developmentaly dissociated processes: prepupal growth and pupal remodeling.More generally, adult morphology alone appears to provide few clues, if any, as to the relative contributions of both processes to the expression of alternative male morphs, underscoring the importance of developmental studies in efforts aimed at understanding the evolution of adult diversity patterns.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, Indiana University, Bloomington IN, USA. armin@indiana.edu.

ABSTRACT

Background: How novel morphological traits originate and diversify represents a major frontier in evolutionary biology. Horned beetles are emerging as an increasingly popular model system to explore the genetic, developmental, and ecological mechanisms, as well as the interplay between them, in the genesis of novelty and diversity. The horns of beetles originate during a rapid growth phase during the prepupal stage of larval development. Differential growth during this period is either implicitly or explicitly assumed to be the sole mechanism underlying differences in horn expression within and between species. Here I focus on male horn dimorphisms, a phenomenon at the center of many studies in behavioral ecology and evolutionary development, and quantify the relative contributions of a previously ignored developmental process, pupal remodeling, to the expression of male dimorphism in three horned beetle species.

Results: Prepupal growth is not the only determinant of differences in male horn expression. Instead, following their initial prepupal growth phase, beetles may be extensively remodeled during the subsequent pupal stage in a sex and size-dependent manner. Specifically, male dimorphism in the three Onthophagus species studied here was shaped not at all, partly or entirely by such pupal remodeling rather than differential growth, suggesting that pupal remodeling is phylogenetically widespread, evolutionarily labile, and developmentally flexible.

Conclusion: This study is the first to document that male dimorphism in horned beetles is the product of two developmentaly dissociated processes: prepupal growth and pupal remodeling. More generally, adult morphology alone appears to provide few clues, if any, as to the relative contributions of both processes to the expression of alternative male morphs, underscoring the importance of developmental studies in efforts aimed at understanding the evolution of adult diversity patterns.

Show MeSH
Related in: MedlinePlus