Heterochrony and developmental timing mechanisms: changing ontogenies in evolution

Abstract

Heterochrony, or a change in developmental timing, is an important mechanism of evolutionary change. Historically the concept of heterochrony has focused alternatively on changes in size and shape or changes in developmental sequence, but most have focused on the pattern of change. Few studies have examined changes in the mechanisms that embryos use to actually measure time during development. Recently, evolutionary studies focused on changes in distinct timekeeping mechanisms have appeared, and this review examines two such case studies: the evolution of increased segment number in snakes and the extreme rostral to caudal gradient of developmental maturation in marsupials. In both examples, heterochronic modifications of the somite clock have been important drivers of evolutionary change.

Keywords: Developmental timing; Heterochrony; Limb; Marsupial; Somitogenesis; Timekeeping mechanisms.

Figure 1

Somitogenesis compared between different vertebrate models. In the corn snake, more stripes of cyclic gene expression are seen simultaneously in the presomitic mesoderm and many more smaller-sized somites are formed because the rate of the somite clock is accelerated. Dotted line indicates the position of the determination front. Anterior is to the top, posterior to the bottom. PSM, presomitic mesoderm. Redrawn from [48].

Figure 2

Alcian blue and alizarin red skeletal preparations of an E14 mouse (A) and a two day old opossum (B). Bone is red and cartilage is blue. Modified from [51].

Figure 3

Somitogenesis rate in opossum decreases 4-fold from rostral to caudal, slowing to greater extent than the caudal rate for mouse. Opossum embryo is stained with antibody to neurofilament to highlight spinal nerves. FL indicates forelimb; HL indicates hindlimb. Mouse data from [97].

Figure 4

A, stage 24 somite-matched opossum embryos hybridized with in situ probe to Lnfg. Three different phases of cyclic gene expression can be seen in the presomitic mesoderm. B, stage 22 opossum embryo hybridized with Tbx5 probe and shown with first two somites highlighted by dotted lines. At this stage the first somites form and the forelimb field is specified. C, stage 23 opossum embryo hybridized with probe to Mesp2, a gene that defines the future segmental boundary. D, stage 26 opossum embryo hybridized with Pax3 probe. Pax3 positive myocytes can be seen leaving the somites and migrating into the forelimb. Note that more anterior myocytes have migrated further from the somites than more posterior myocytes. Anterior and posterior limits of the forelimb bud are indicated by the dashed lines. E, stage 28 opossum embryo hybridized with Pax3 probe. Asterisk indicates a stream of myocytes en route to the future tongue. Note the difference in the size of the fore- and hindlimb buds. F, opossum embryo stained with antibody to neurofilament. Note the gradient in spinal nerve maturation and outgrowth from rostral to caudal. G, newborn opossum crawling. Anterior is to the top. fl, forelimb; hl, hindlimb.