Limb Evolution: Fish fins or tetrapod limbs — a simple twist of fate?

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Limb Evolution: Fish fins or tetrapod limbs — a simple twist of fate? Michael I. Coates  Current Biology  Volume 5, Issue 8, Pages 844-848 (August 1995) DOI: 10.1016/S0960-9822(95)00169-2

Figure 1 (a) Regions of Hoxa-11 expression in the mouse forelimb (adapted from [1]) and Hoxd-11 expression in the chick hindlimb (adapted from [2]) are shown in dark blue; non-expressing regions of mesenchyme are shaded light blue. Note that by equivalent stages of development in the two species (‘stage t2’), the Hoxa-11 distal expression boundary lies proximal to the ‘autopodal’ region (including distal carpals and digits), and that Hoxd-11 is now expressed antero-posteriorly, across the sub-apical mesenchyme (AER, apical ectodermal ridge; ec, ectoderm; mc, mesenchyme). (b)Hoxa-11 and Hoxd-12 expression (dark blue) in the zebrafish pectoral fin (adapted from [1]). In contrast to the amniote limb expression patterns, at the t1 stage, Hoxa-11 is expressed predominantly in the posterior region, and at t2 there is no significant distal zone of non-expression. Hoxd-12 expression remains in the posterior half of the developing fin bud; by 58 hours post-fertilization (hpf) the expression is weakening (aef, apical ectodermal fin fold). (c)Hoxd-12 and shh expression (dark blue) in budding pelvic fins (adapted from [1]). Both expression patches are confined to the posterior zone, and neither reaches the most distal mesenchymal cells. dpf, days post-fertilization. (d) Lateroventral views of near-adult pectoral and pelvic fin and girdle skeletons, with dermal fin rays omitted. Camera lucida drawing of a cleared and stained zebrafish specimen (Danio rerio): blue, dermal bone; green, endoskeletal bone and cartilage (cl, cleithrum; pp, pelvic plate; sc, scapulocoracoid plate; R, proximal radials; r, distal radials). Distal is to the top and anterior to the left in all panels. Current Biology 1995 5, 844-848DOI: (10.1016/S0960-9822(95)00169-2)

Figure 1 (a) Regions of Hoxa-11 expression in the mouse forelimb (adapted from [1]) and Hoxd-11 expression in the chick hindlimb (adapted from [2]) are shown in dark blue; non-expressing regions of mesenchyme are shaded light blue. Note that by equivalent stages of development in the two species (‘stage t2’), the Hoxa-11 distal expression boundary lies proximal to the ‘autopodal’ region (including distal carpals and digits), and that Hoxd-11 is now expressed antero-posteriorly, across the sub-apical mesenchyme (AER, apical ectodermal ridge; ec, ectoderm; mc, mesenchyme). (b)Hoxa-11 and Hoxd-12 expression (dark blue) in the zebrafish pectoral fin (adapted from [1]). In contrast to the amniote limb expression patterns, at the t1 stage, Hoxa-11 is expressed predominantly in the posterior region, and at t2 there is no significant distal zone of non-expression. Hoxd-12 expression remains in the posterior half of the developing fin bud; by 58 hours post-fertilization (hpf) the expression is weakening (aef, apical ectodermal fin fold). (c)Hoxd-12 and shh expression (dark blue) in budding pelvic fins (adapted from [1]). Both expression patches are confined to the posterior zone, and neither reaches the most distal mesenchymal cells. dpf, days post-fertilization. (d) Lateroventral views of near-adult pectoral and pelvic fin and girdle skeletons, with dermal fin rays omitted. Camera lucida drawing of a cleared and stained zebrafish specimen (Danio rerio): blue, dermal bone; green, endoskeletal bone and cartilage (cl, cleithrum; pp, pelvic plate; sc, scapulocoracoid plate; R, proximal radials; r, distal radials). Distal is to the top and anterior to the left in all panels. Current Biology 1995 5, 844-848DOI: (10.1016/S0960-9822(95)00169-2)

Figure 1 (a) Regions of Hoxa-11 expression in the mouse forelimb (adapted from [1]) and Hoxd-11 expression in the chick hindlimb (adapted from [2]) are shown in dark blue; non-expressing regions of mesenchyme are shaded light blue. Note that by equivalent stages of development in the two species (‘stage t2’), the Hoxa-11 distal expression boundary lies proximal to the ‘autopodal’ region (including distal carpals and digits), and that Hoxd-11 is now expressed antero-posteriorly, across the sub-apical mesenchyme (AER, apical ectodermal ridge; ec, ectoderm; mc, mesenchyme). (b)Hoxa-11 and Hoxd-12 expression (dark blue) in the zebrafish pectoral fin (adapted from [1]). In contrast to the amniote limb expression patterns, at the t1 stage, Hoxa-11 is expressed predominantly in the posterior region, and at t2 there is no significant distal zone of non-expression. Hoxd-12 expression remains in the posterior half of the developing fin bud; by 58 hours post-fertilization (hpf) the expression is weakening (aef, apical ectodermal fin fold). (c)Hoxd-12 and shh expression (dark blue) in budding pelvic fins (adapted from [1]). Both expression patches are confined to the posterior zone, and neither reaches the most distal mesenchymal cells. dpf, days post-fertilization. (d) Lateroventral views of near-adult pectoral and pelvic fin and girdle skeletons, with dermal fin rays omitted. Camera lucida drawing of a cleared and stained zebrafish specimen (Danio rerio): blue, dermal bone; green, endoskeletal bone and cartilage (cl, cleithrum; pp, pelvic plate; sc, scapulocoracoid plate; R, proximal radials; r, distal radials). Distal is to the top and anterior to the left in all panels. Current Biology 1995 5, 844-848DOI: (10.1016/S0960-9822(95)00169-2)

Figure 1 (a) Regions of Hoxa-11 expression in the mouse forelimb (adapted from [1]) and Hoxd-11 expression in the chick hindlimb (adapted from [2]) are shown in dark blue; non-expressing regions of mesenchyme are shaded light blue. Note that by equivalent stages of development in the two species (‘stage t2’), the Hoxa-11 distal expression boundary lies proximal to the ‘autopodal’ region (including distal carpals and digits), and that Hoxd-11 is now expressed antero-posteriorly, across the sub-apical mesenchyme (AER, apical ectodermal ridge; ec, ectoderm; mc, mesenchyme). (b)Hoxa-11 and Hoxd-12 expression (dark blue) in the zebrafish pectoral fin (adapted from [1]). In contrast to the amniote limb expression patterns, at the t1 stage, Hoxa-11 is expressed predominantly in the posterior region, and at t2 there is no significant distal zone of non-expression. Hoxd-12 expression remains in the posterior half of the developing fin bud; by 58 hours post-fertilization (hpf) the expression is weakening (aef, apical ectodermal fin fold). (c)Hoxd-12 and shh expression (dark blue) in budding pelvic fins (adapted from [1]). Both expression patches are confined to the posterior zone, and neither reaches the most distal mesenchymal cells. dpf, days post-fertilization. (d) Lateroventral views of near-adult pectoral and pelvic fin and girdle skeletons, with dermal fin rays omitted. Camera lucida drawing of a cleared and stained zebrafish specimen (Danio rerio): blue, dermal bone; green, endoskeletal bone and cartilage (cl, cleithrum; pp, pelvic plate; sc, scapulocoracoid plate; R, proximal radials; r, distal radials). Distal is to the top and anterior to the left in all panels. Current Biology 1995 5, 844-848DOI: (10.1016/S0960-9822(95)00169-2)

Figure 2 (a) Selected adult pectoral fin endoskeletal patterns plotted on a cladogram of major groups of bony fish (Osteichthyes;† extinct taxon). The axes of the metapterygia are indicated with a red line; in the zebrafish, the metapterygial course is speculative, and differs from that suggested by Sordino et al.[1]. In fact, there may be a significant difference in the morphological assembly of metapterygia between lobe-finned fish (Sarcopterygii) and other jawed vertebrates, including ray-finned fish (Actinopterygii). In the former, the metapterygia appear to consist of coalesced proximal radials; in the latter, metapterygia derive from a single proximal focal condensation. Zebrafish skeleton redrawn from [1]; for others see [6] and references therein. A provisional hypothesis of paired fin developmental characteristics is mapped onto the cladogram. (b) Prechondrogenic cell clusters (blue) segmenting to form endoskeleton in a chondrostean pelvic fin. The posterior-most clusters form a 1:2 branching pattern characteristic of the metapterygium, superimposed with the segmentation and bifurcation pattern (dark grey; note the close correspondence between the metaptarygial development zone in this fin bud and the posterior pelvic fin bud expression patch in Figure 1c). Differentiation proceeds from posterior to anterior of the fin base (redrawn from [6]). (c) Shubin and Alberch's [4] scheme of tetrapod (amniote) limb skeletal pattern development. Blue shapes represent prechondrogenic cell clusters, dotted lines indicate cellular connections. Development proceeds in a proximo-distal direction. In comparison with the short pelvic fin metapterygium, the branched and segmented limb axis extends antero-distally to form the digital arch (dark grey). The anterior edges of all fins and limbs are to the left. Current Biology 1995 5, 844-848DOI: (10.1016/S0960-9822(95)00169-2)

Figure 2 (a) Selected adult pectoral fin endoskeletal patterns plotted on a cladogram of major groups of bony fish (Osteichthyes;† extinct taxon). The axes of the metapterygia are indicated with a red line; in the zebrafish, the metapterygial course is speculative, and differs from that suggested by Sordino et al.[1]. In fact, there may be a significant difference in the morphological assembly of metapterygia between lobe-finned fish (Sarcopterygii) and other jawed vertebrates, including ray-finned fish (Actinopterygii). In the former, the metapterygia appear to consist of coalesced proximal radials; in the latter, metapterygia derive from a single proximal focal condensation. Zebrafish skeleton redrawn from [1]; for others see [6] and references therein. A provisional hypothesis of paired fin developmental characteristics is mapped onto the cladogram. (b) Prechondrogenic cell clusters (blue) segmenting to form endoskeleton in a chondrostean pelvic fin. The posterior-most clusters form a 1:2 branching pattern characteristic of the metapterygium, superimposed with the segmentation and bifurcation pattern (dark grey; note the close correspondence between the metaptarygial development zone in this fin bud and the posterior pelvic fin bud expression patch in Figure 1c). Differentiation proceeds from posterior to anterior of the fin base (redrawn from [6]). (c) Shubin and Alberch's [4] scheme of tetrapod (amniote) limb skeletal pattern development. Blue shapes represent prechondrogenic cell clusters, dotted lines indicate cellular connections. Development proceeds in a proximo-distal direction. In comparison with the short pelvic fin metapterygium, the branched and segmented limb axis extends antero-distally to form the digital arch (dark grey). The anterior edges of all fins and limbs are to the left. Current Biology 1995 5, 844-848DOI: (10.1016/S0960-9822(95)00169-2)

Figure 2 (a) Selected adult pectoral fin endoskeletal patterns plotted on a cladogram of major groups of bony fish (Osteichthyes;† extinct taxon). The axes of the metapterygia are indicated with a red line; in the zebrafish, the metapterygial course is speculative, and differs from that suggested by Sordino et al.[1]. In fact, there may be a significant difference in the morphological assembly of metapterygia between lobe-finned fish (Sarcopterygii) and other jawed vertebrates, including ray-finned fish (Actinopterygii). In the former, the metapterygia appear to consist of coalesced proximal radials; in the latter, metapterygia derive from a single proximal focal condensation. Zebrafish skeleton redrawn from [1]; for others see [6] and references therein. A provisional hypothesis of paired fin developmental characteristics is mapped onto the cladogram. (b) Prechondrogenic cell clusters (blue) segmenting to form endoskeleton in a chondrostean pelvic fin. The posterior-most clusters form a 1:2 branching pattern characteristic of the metapterygium, superimposed with the segmentation and bifurcation pattern (dark grey; note the close correspondence between the metaptarygial development zone in this fin bud and the posterior pelvic fin bud expression patch in Figure 1c). Differentiation proceeds from posterior to anterior of the fin base (redrawn from [6]). (c) Shubin and Alberch's [4] scheme of tetrapod (amniote) limb skeletal pattern development. Blue shapes represent prechondrogenic cell clusters, dotted lines indicate cellular connections. Development proceeds in a proximo-distal direction. In comparison with the short pelvic fin metapterygium, the branched and segmented limb axis extends antero-distally to form the digital arch (dark grey). The anterior edges of all fins and limbs are to the left. Current Biology 1995 5, 844-848DOI: (10.1016/S0960-9822(95)00169-2)