Isometric contractile properties of sexually dimorphic forelimb muscles in the marine toad Bufo marinus Linnaeus 1758: functional analysis and implications for amplexus

Abstract

It has been shown in the bullfrog, Rana catesbeiana Shaw 1802, that certain forelimb muscles in males have different contractile properties when compared with females, which may result from adaptation for amplexus. We extended this study to a distantly related species, Bufo marinus Linnaeus 1758, by testing the isometric contractile properties of three muscles, abductor indicus longus (AIL), and flexor carpi radialis (FCR) (both dimorphic muscles), and extensor carpi ulnaris (ECU) (nondimorphic control). In males the dimorphic muscles had greater wet mass and cross-sectional area than in the females, and also produced significantly greater isometric force. As in bullfrogs, however, the maximum tetanic force per cm 2 of muscle cross-section did not differ between the sexes. In spite of this similarity in maximum force, the two dimorphic muscles were much less fatigable in the males than in the females. Lower fatigability in males correlated with exceptionally elongated relaxation times that maintained high levels of force between stimulus trains. This sustained force was negligible in the females, suggesting that this feature may allow males to maintain amplexus for prolonged periods. The same sustained force response was observed in the earlier study of Rana catesbeiana. Because this response is similar in Bufo and Rana, muscular properties correlated with amplexus may be shared across anurans by inheritance of this response from a common ancestor.

Sexual dimorphism of extensor carpi radialis muscle size, isometric force, relaxation rate and stamina during the breeding season of the frogRana temporariaLinnaeus 1758

“…However, twitch relaxation times were significantly slower in male than in female abductor indicus longus (AIL) and flexor carpi radialis (FCR) muscle (Peters and Aulner, 2000). Similar (although non-significant) trends in twitch relaxation times, but significantly slower tetanus relaxation times, in male than in female AIL and FCR in Bufo marinus outside of the reproductive season were also found (Clark and Peters, 2006). Peters and Aulner (Peters and Aulner, 2000) found much faster ECR relaxation times in male Rana catesbeiana than we found in male Rana temporaria but these differences may again reflect differences in reproductive state between the two studies; indeed the contractile properties of flexor carpi radialis muscle tend to become faster outside of the breeding season (Melichna et al, 1972).…”

“…This slower relaxation in males led to very limited relaxation (sustained force) between tetani during the fatigue run, such that the male ECR muscle could maintain almost constant isometric force when stimulated for only one fifth of the time (for 200·ms in every 1·s). Previous studies on anuran dimorphic forearm muscles outside of the reproductive season have also reported a higher sustained force in males than in females (Clark and Peters, 2006;Peters and Aulner, 2000) temporaria was 94% longer (slower) in males than in females during the breeding season and such large differences persisted throughout the year, with muscle in males possessing more fibres with low myosin ATPase activity (Melichna et al, 1972). Peters and Aulner found ECR twitch relaxation times were 52% slower in male than in female Rana catesbeiana outside of the reproductive season, although these values did not reach the level of significance (Peters and Aulner, 2000).…”

“…The prevalence of amplexus as an important stage of the reproductive mode of anurans has resulted in the evolution of sexual dimorphism in the forelimb muscles of anurans (Clark and Peters, 2006;Oka et al, 1984;Peters and Aulner, 2000;Sidor and Blackburn, 1998;Yekta and Blackburn, 1992). Some forelimb muscles such as extensor carpi radialis, flexor carpi radialis, sternoradialis and abductor indicus longus that are involved in amplexus have been found to be larger in mass and cross-sectional area in male than in female frogs (Clark and Peters, 2006;Kirby, 1983;Oka et al, 1984;Peters and Aulner, 2000;Yekta and Blackburn, 1992) and to have more oxidative fibers and/or higher oxidative capacity in males than in females (Kirby, 1983;Melichna et al, 1972;Peters, 2001;Rubinstein et al, 1983) (but see Oka et al, 1984).…”

“…Some forelimb muscles such as extensor carpi radialis, flexor carpi radialis, sternoradialis and abductor indicus longus that are involved in amplexus have been found to be larger in mass and cross-sectional area in male than in female frogs (Clark and Peters, 2006;Kirby, 1983;Oka et al, 1984;Peters and Aulner, 2000;Yekta and Blackburn, 1992) and to have more oxidative fibers and/or higher oxidative capacity in males than in females (Kirby, 1983;Melichna et al, 1972;Peters, 2001;Rubinstein et al, 1983) (but see Oka et al, 1984). Such differences in muscle morphology have been found to lead to higher absolute isometric force in male muscles, without a difference in isometric stress (force per cross-sectional area) between sexes in two distantly related species, Rana catesbeiana and Bufo marinus (Clark and Peters, 2006;Peters and Aulner, 2000). However, these previous studies did not compare muscle mechanics during the reproductive season, but did propose that sexual dimorphism probably increases during the reproductive phase of males.…”

No sexual dimorphism in limb muscles of a frog not engaging in amplexus

“…Males have much more robust forelimbs than females, even though the females are larger in body size (Kirby, 1983;Oka et al, 1984;Yekta & Blackburn, 1992;Peters & Aulner, 2000;Lee, 2001;Clark & Peters, 2006;Navas & James, 2007;Liao et al, 2012a;Mi, 2012). The cause of this sexual divergence is generally thought to be associated with amplexus: the common mating strategy in anurans where the male typically mounts the female and adopts a "clasping" posture while awaiting and during oviposition (Duellman, 1992;Lee, 2001).…”