The Evolutionary and Developmental Basis of Parallel Reduction in Mammalian Zeugopod Elements

Abstract

Understanding the mechanisms by which parallel evolution occurs has the potential to clarify the complex relationship between evolution and development. In this study, we examine the role of development in the repeated reduction of zeugopod elements during mammalian evolution, a functionally important phenomenon enabling locomotor specialization. By completing a morphometric study (incorporating both analyses of variation and phylogenetics) of mammalian limbs, we are able to demonstrate an evolutionary trend toward width reduction in posterior zeugopod elements of the forelimbs and hindlimbs, the ulna and fibula, respectively. We also examine the developmental basis of limb reduction in three test cases, the bat Carollia perspicillata ulna and fibula and the mouse Mus musculus fibula. The most common pattern of reduction, that of reduced element width, was achieved via the same developmental process in both bat and mouse limbs (i.e., by a slower growth rate relative to other skeletal elements), suggesting that the parallel reduction of the posterior zeugopod element within mammals could have occurred primarily by the repeated evolution of the same developmental mechanism. However, our findings also suggest that the developmental mechanisms behind the parallel evolution of other, more taxon-specific characteristics of limb reduction (i.e., element fusion) are not conserved.

Hox11 genes establish synovial joint organization and phylogenetic characteristics in developing mouse zeugopod skeletal elements

“…Mutant zeugopod elements were hypomorphic and entirely cartilaginous ( Fig. 1G-J, arrows), had lost their morphologic distinction in terms of length and width (Coates et al, 2002;Sears et al, 2007) and displayed elbow and knee joints with novel characteristics (Fig. 1H,K).…”

Molecular Determinants of Bat Wing Development

“…Embryological data from Carollia perspicillata demonstrate that the initial mesenchymal condensation of the bat ulna is similar in size to that of the bat radius [Sears et al, 2007]. The subsequent reduction of the bat ulna (relative to the radius) occurs in three stages.…”

“…Chiropterans are not the only mammalian order to reduce zeugopod skeletal elements -at least 11 of the 18 eutherian orders exhibit zeugopod reduction relative to the ancestral eutherian condition. Within the zeugopod, mammals reduce the posterior elements (the ulna and fibula) significantly more frequently than the anterior elements (the radius and tibia) [Sears et al, 2007], as is the case in bats.…”

Postnatal Bone Elongation of the Manus versus Pes: Analysis of the Chondrocytic Differentiation Cascade in <i>Mus musculus</i> and <i>Eptesicus fuscus</i>

“…A particularly interesting group in this respect are Chiroptera, a group with extreme functional divergence for specialization of hindlimb versus forelimb use. The fossil record offers minimal clues about the evolution of bat digital specialization, other than to establish the abrupt appearance of multiple bat species as the only true flying mammals, now constituting approximately 20% of all existing mammalian species [Stanhope et al, 1992;Thewissen and Babcock, 1992;Shubin et al, 1997;Simmons and Geisler, 1998;Valentine et al, 1999;Speakman, 2001;Logan, 2003;Teeling et al, 2000Teeling et al, , 2005Popovici et al, 2005;Kiefer, 2006;Sears et al, 2006Sears et al, , 2007.…”

“…Most recently the idea has emerged that, given the power of transgenic technology and the adaptability of the mouse for creation of transgenic constructs, it might be possible to utilize gene manipulation to develop a molecular engineering approach to mimic key genetic shifts that have occurred to allow for the rapid adaptive radiation of a given group during evolution [Hérault et al, 1997;Cubo et al, 2000;Fondon and Garner, 2004;Sears et al, 2006Sears et al, , 2007. A particularly interesting group in this respect are Chiroptera, a group with extreme functional divergence for specialization of hindlimb versus forelimb use.…”