Heterochrony in the regulation of the developing marsupial limb

Abstract

Background: At birth, marsupial neonates have precociously developed forelimbs. The development of the tammar wallaby (Macropus eugenii) hindlimbs lags significantly behind that of the forelimbs. This differs from the grey short-tailed opossum, Monodelphis domestica, which has relatively similar fore-and hindlimbs at birth. This study examines the expression of the key patterning genes TBX4, TBX5, PITX1, FGF8, and SHH in developing limb buds in the tammar wallaby. Results: All genes examined were highly conserved with orthologues from opossum and mouse. TBX4 expression appeared earlier in development than in the mouse, but later than in the opossum. SHH expression is restricted to the zone of polarising activity, while TBX5 (forelimb) and PITX1 (hindlimb) showed diffuse mRNA expression. FGF8 is specifically localised to the apical ectodermal ridge, which is more prominent than in the opossum. Conclusions: The most marked divergence in limb size in marsupials occurs in the kangaroos and wallabies. The faster development of the fore limb compared to that of the hind limb correlates with the early timing of the expression of the key patterning genes in these limbs. Developmental Dynamics 243:324-338, 2014. V C 2013 Wiley Periodicals, Inc.Key words: heterochrony; marsupial limb; species-specific differences Key Findings:There is high conservation of all genes examined with the mouse and opossum orthologues The AER in the tammar is more prominent than in the opossum limb TBX5 expression is only slightly earlier in tammar when compared to the mouse The faster development of the fore limb compared to that of the hind limb correlates with the early timing of the expression of the key patterning genes in these limbs.

The significance and scope of evolutionary developmental biology: a vision for the 21st century

“…Integrating development into the fossil record has been used to explain the origins of mammalian flight , the loss of limbs in snakes (Cohn and Tickle 1999;Di-Po€ ı et al 2010;Mallo et al 2010;Head and Polly 2015), cetaceans (Thewissen et al 2006), and fish (Shapiro et al 2004;Tanaka et al 2005), as well as the mechanisms of marsupial forelimb heterochronies (Doroba and Sears 2010;Keyte and Smith 2010;Chew et al 2014). Integrating development into the fossil record has been used to explain the origins of mammalian flight , the loss of limbs in snakes (Cohn and Tickle 1999;Di-Po€ ı et al 2010;Mallo et al 2010;Head and Polly 2015), cetaceans (Thewissen et al 2006), and fish (Shapiro et al 2004;Tanaka et al 2005), as well as the mechanisms of marsupial forelimb heterochronies (Doroba and Sears 2010;Keyte and Smith 2010;Chew et al 2014).…”

“…Limb evolution also has been a critical success story for the integration of paleontology and evo-devo. Integrating development into the fossil record has been used to explain the origins of mammalian flight , the loss of limbs in snakes (Cohn and Tickle 1999;Di-Po€ ı et al 2010;Mallo et al 2010;Head and Polly 2015), cetaceans (Thewissen et al 2006), and fish (Shapiro et al 2004;Tanaka et al 2005), as well as the mechanisms of marsupial forelimb heterochronies (Doroba and Sears 2010;Keyte and Smith 2010;Chew et al 2014). The combination of paleontology and evo-devo has also helped explain the homology of digits between dinosaurs and birds (Tamura et al 2011;Wang et al 2011;Salinas-Saavedra et al 2014) as well as their skulls (Bhullar et al 2012).…”

Comparative Myology and Evolution of Marsupials and Other Vertebrates, With Notes on Complexity, Bauplan, and “Scala Naturae”

“…Marsupial opossums (order Didelphimorpha) are frequently the focus of evolutionary developmental studies because this order is the sister-group of a clade including all other extant marsupials and is therefore a good model to study the origin and early evolution of marsupials as a whole (e.g., Horovitz and S anchez-Villagra, 2003). Moreover, opossums are a very useful model to investigate the diversity of mammalian development because marsupials share very peculiar developmental features that are not seen in placentals, many of which are related to remarkable heterochronic and heterotopic changes in marsupials (Smith, , 2001(Smith, , 2006S anchez-Villagra et al, 2002;Vaglia and Smith, 2003;Sears, 2004;Keyte and Smith, 2010;Kelly and Sears, 2011;Moustakas et al, 2011;Goswami et al, 2012;H€ ubler et al, 2013;Wakamatsu et al, 2014;Chew et al, 2014). Interestingly, despite these marked developmental differences, the skeletal structures of adult marsupials such as opossums and placentals such as mice are, in general, quite similar (e.g., Smith 2006;Goswami et al, 2012).…”

Hormone-Independent Pathways of Sexual Differentiation

“…Nevertheless, the young climbs to the pouch using its well-developed forelimbs (FL) unaided by the mother, seeks out, and attaches itself to one of the 4 available teats (T). Note the under-developed hindlimbs (HL) [see Chew et al, 2013b] and the pouch scale (Ps). The young remains permanently attached for about the first 5 months, but intermittently releases the teat after that until pouch exit around 9 months after birth.…”