Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks

Abstract

Hindlimb loss has evolved repeatedly in many different animals by means of molecular mechanisms that are still unknown. To determine the number and type of genetic changes underlying pelvic reduction in natural populations, we carried out genetic crosses between threespine stickleback fish with complete or missing pelvic structures. Genome-wide linkage mapping shows that pelvic reduction is controlled by one major and four minor chromosome regions. Pitx1 maps to the major chromosome region controlling most of the variation in pelvic size. Pelvic-reduced fish show the same left-right asymmetry seen in Pitx1 knockout mice, but do not show changes in Pitx1 protein sequence. Instead, pelvic-reduced sticklebacks show site-specific regulatory changes in Pitx1 expression, with reduced or absent expression in pelvic and caudal fin precursors. Regulatory mutations in major developmental control genes may provide a mechanism for generating rapid skeletal changes in natural populations, while preserving the essential roles of these genes in other processes.

Postembryonic staging of wild‐type goldfish, with brief reference to skeletal systems

“…Because the spines in some of these Ostariophysan fish equip the venom glands (Wright, 2009), it may be presumed that the segmented fin spines have a protective function against predators; furthermore, its evolution may be related to other environmental factors, akin to the pelvic spines of sticklebacks (Hoogland et al, 1956; Bell, 1987; Bell et al, 1993; Shapiro et al, 2004; Chan et al, 2010). …”

“…Although the evolution and development of the stickleback spine has been well investigated at the molecular level (Shapiro et al, 2004; Chan et al, 2010), little is known of that of Ostariophysan fish; this may be due to the absence of the segmented fin spine in zebrafish (Mabee et al, 2002). At present, the gene(s) responsible for segmented fin spine formation and its divergence in the Ostariophysan fish lineage is (are) unknown.…”

Update on Clubfoot: Etiology and Treatment

“…PITX1 is the first gene implicated in clubfoot that explains the specific involvement of the foot, since PITX1 is expressed nearly exclusively in the hindlimb and is responsible for rapid evolutionary changes in pelvic morphology in lower vertebrates [58]. Specific involvement of the foot also appears to exclude many of the skeletal muscle contractile genes that are responsible for distal arthrogryposis [62,63,65,70] in the causation of idiopathic clubfoot, as mutations in these genes cause both upper and lower extremity involvement and were not identified in idiopathic clubfoot patients [29].…”

Gene(s) and individual feeding behavior: Exploring eco‐evolutionary dynamics underlying left‐right asymmetry in the scale‐eating cichlid fishPerissodus microlepis

“…Linkage rather than a direct causal relationship or a polygenetic basis for mouth asymmetry (as discussed in Raffini et al., 2017) could explain the relatively small proportion of mouth phenotypic variation accounted for by this SNP, including when the geographic variation is considered. Alternatively, the location of this SNP in a putatively non‐coding region flanking two genes might suggest that variation in regulatory and not in coding elements may be responsible for phenotypic variation (as seen in e.g., Belting, Shashikant, & Ruddle, 1998; Chan et al., 2010; Cretekos et al., 2008; Guenther, Tasic, Luo, Bedell, & Kingsley, 2014; Guerreiro et al., 2013; Schneider et al., 2014; Shapiro, Marks, Peichel, & Blackman, 2004). Future investigations focusing on immunity‐related processes or loci underlying this polymorphism might further advance our understanding of the genetic architecture of the P. microlepis head asymmetry.…”