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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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Species used in the present study. (A) Onthophagus nigriventris, (B) O. taurus, and (C) O. binodis. Shown for each species are large horned (major) males (top) and small, hornless (minor) males (bottom) as pupae (left) and corresponding adults (right). Arrows highlight lateral concavity in adult, but not pupal, O. binodis referred to in text.
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Figure 1: Species used in the present study. (A) Onthophagus nigriventris, (B) O. taurus, and (C) O. binodis. Shown for each species are large horned (major) males (top) and small, hornless (minor) males (bottom) as pupae (left) and corresponding adults (right). Arrows highlight lateral concavity in adult, but not pupal, O. binodis referred to in text.

Mentions: I investigated the relative contribution of pupal remodeling in the development and evolution of sexual dimorphisms by quantifying ontogenetic changes in the allometric scaling between body size and horn length from the pupal to the adult stage and the degree to which ontogenetic changes in allometries differed between males as a function of body size. In particular, I examined the ontogeny of male horn dimorphism in three species (Fig. 1). Large adult male O. nigriventris express an enormous thoracic horn, whereas small males express only a small pointy thoracic projection. The transition from small to large horns occurs over a very narrow range of body sizes [58]. O. binodis exhibits the same general pattern, though horn size and degree of male dimorphism are considerably reduced compared to O. nigriventris [37,38]. Lastly, large male O. taurus express two head horns while smaller males remain female-like and largely hornless [59]. Males of all three species use their horns in male fights over access to females, where they function as jousting devices during head-to-head combat and to block entrances to breeding tunnels [38,58,60].


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

Moczek AP - BMC Evol. Biol. (2007)

Species used in the present study. (A) Onthophagus nigriventris, (B) O. taurus, and (C) O. binodis. Shown for each species are large horned (major) males (top) and small, hornless (minor) males (bottom) as pupae (left) and corresponding adults (right). Arrows highlight lateral concavity in adult, but not pupal, O. binodis referred to in text.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Species used in the present study. (A) Onthophagus nigriventris, (B) O. taurus, and (C) O. binodis. Shown for each species are large horned (major) males (top) and small, hornless (minor) males (bottom) as pupae (left) and corresponding adults (right). Arrows highlight lateral concavity in adult, but not pupal, O. binodis referred to in text.
Mentions: I investigated the relative contribution of pupal remodeling in the development and evolution of sexual dimorphisms by quantifying ontogenetic changes in the allometric scaling between body size and horn length from the pupal to the adult stage and the degree to which ontogenetic changes in allometries differed between males as a function of body size. In particular, I examined the ontogeny of male horn dimorphism in three species (Fig. 1). Large adult male O. nigriventris express an enormous thoracic horn, whereas small males express only a small pointy thoracic projection. The transition from small to large horns occurs over a very narrow range of body sizes [58]. O. binodis exhibits the same general pattern, though horn size and degree of male dimorphism are considerably reduced compared to O. nigriventris [37,38]. Lastly, large male O. taurus express two head horns while smaller males remain female-like and largely hornless [59]. Males of all three species use their horns in male fights over access to females, where they function as jousting devices during head-to-head combat and to block entrances to breeding tunnels [38,58,60].

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