Assessing Species-specific Contributions To Craniofacial Development Using Quail-duck Chimeras

Abstract

The generation of chimeric embryos is a widespread and powerful approach to study cell fates, tissue interactions, and species-specific contributions to the histological and morphological development of vertebrate embryos. In particular, the use of chimeric embryos has established the importance of neural crest in directing the species-specific morphology of the craniofacial complex. The method described herein utilizes two avian species, duck and quail, with remarkably different craniofacial morphology. This method greatly facilitates the investigation of molecular and cellular regulation of species-specific pattern in the craniofacial complex. Experiments in quail and duck chimeric embryos have already revealed neural crest-mediated tissue interactions and cell-autonomous behaviors that regulate species-specific pattern in the craniofacial skeleton, musculature, and integument. The great diversity of neural crest derivatives suggests significant potential for future applications of the quail-duck chimeric system to understanding vertebrate development, disease, and evolution.

Cellular Control of Time, Size, and Shape in Development and Evolution

“…In particular, additional details on molecular and cellular mechanisms through which the craniofacial skeleton acquires its proper size and shape have come from our studies, using a unique avian chimeric transplantation system that exploits species-specific differences between Japanese quail and white Pekin duck , 2007Lwigale and Schneider 2008;Jheon and Schneider 2009;Ealba and Schneider 2013;Fish and Schneider 2014b).…”

Neural crest and the origin of species‐specific pattern

“…By the turn of the 21th Century, other transplant experiments in non-amphibian taxa such as among mouse, human, chick, or quail (Cohen et al, 2016;Fontaine-Perus, 2000;Fontaine-Perus & Cheraud, 2005;Fontaine-Perus, Cheraud, & Halgand, 1996;Fontaine-Perus et al, 1997;Kirby, Stadt, Kumiski, & Herlea, 2000;Lwigale & Schneider, 2008;Mitsiadis, Caton, & Cobourne, 2006;Mitsiadis, Cheraud, Sharpe, & Fontaine-Perus, 2003;Pudliszewski & Pardanaud, 2005;Serbedzija & McMahon, 1997); among divergent species of birds including quail, chick, duck, and emu (Ealba et al, 2015;Eames & Schneider, 2005Fish & Schneider, 2014a, 2014bFish, Sklar, Woronowicz, & Schneider, 2014;Hall et al, 2014;Jheon & Schneider, 2009;Le Douarin, Dieterlen-Lievre, Teillet, & Ziller, 2000;Merrill, Eames, Weston, Heath, & Schneider, 2008;Schneider, 2005Schneider, , 2015Sohal, 1976;Solem, Eames, Tokita, & Schneider, 2011;Tokita & Schneider, 2009;Tucker & Lumsden, 2004;Woronowicz, Gline, Herfat, Fields, & Schneider, 2018;Yamashita & Sohal, 1986); as well as between Mexican cavefish and surface fish (Yoshizawa, Hixon, & Jeffery, 2018), reinforced the conclusion that species-specific pattern in the craniofacial complex is largely driven by the neural crest. Harrison (1969) argued that such an ability is due to "congenital specific factors" that "control the relative growth rate" (p. 31) of grafts.…”

“…The success of the quail-chick chimeric system stems from the fact that in general, avian embryos are easily accessible in ovo for all kinds of experimental manipulations. This includes grafting or extirpation of tissues through microsurgery, labeling of cells for lineage analysis, implantation of reagent-soaked beads, injection of biochemicals, and manipulation of gene expression via retroviral infection or electroporation (Cerny, Lwigale, et al, 2004;Chen et al, 1999;Ealba et al, 2015;Eichele, Tickle, & Alberts, 1984;Fekete & Cepko, 1993;Fish & Schneider, 2014a;Fish et al, 2014;Hall et al, 2014;Johnston, 1966;Krull, 2004;Kulesa, Bronner-Fraser, & Fraser, 2000;Larsen, Zeltser, & Lumsden, 2001;Logan & Tabin, 1998;Lwigale, Conrad, & Bronner-Fraser, 2004;Lwigale, Cressy, & Bronner-Fraser, 2005;Lwigale & Schneider, 2008;Momose et al, 1999;Nakamura & Funahashi, 2001;Noden, 1975;Schneider et al, 2001;Serbedzija, Bronner-Fraser, & Fraser, 1989;Stocker, Brown, & Ciment, 1993;Woronowicz et al, 2018). One advantage of working in birds is that after surgery or other manipulations, eggs can simply be resealed and incubated until the embryos reach stages appropriate for further analysis.…”

“…The quail-duck chimeric transplant system has been especially useful for identifying the molecular and cellular basis for species-specific aspects of pattern and for illuminating the mechanistic contributions of neural crest cells during tissue interactions that facilitate the structural and functional integration of the craniofacial complex (Figure 1b,c). The system itself combines classical grafting techniques and tools in vertebrate embryology that have already been mentioned (e.g., Andres, 1949;Hamburger, 1942;Harrison, 1917Harrison, , 1921Harrison, , 1924Harrison, , 1929Harrison, , 1935Spemann, 1918Spemann, , 1921Spemann, , 1938Spemann & Mangold, 1924;Spemann & Schotte, 1932;Twitty, 1934Twitty, , 1945Twitty & Schwind, 1931;Waddington, 1930Waddington, , 1932Wagner, 1959) with modern molecular and cellular methods and assays (Ealba & Schneider, 2013;Fish & Schneider, 2014a;Lwigale & Schneider, 2008). In short, presumptive neural crest cells from the midbrain and anterior hindbrain are transplanted from either quail to duck to create chimeric "quck" or from duck to quail to make chimeric "duail" (Ealba & Schneider, 2013;Fish & Schneider, 2014a;Lwigale & Schneider, 2008; ( Figure 1d).…”

Pericyte ontogeny: the use of chimeras to track a cell lineage of diverse germ line origins

“…10. Videos of two applications of the avian chimera technique, described in an earlier protocol relative to whole neural tube grafts [78], are freely available at https://www.jove.com/video/52514/ and https://www.jove.com/video/51534 [59,81]. 16.…”