TY - JOUR
T1 - Dissection of the complex genetic basis of craniofacial anomalies using haploid genetics and interspecies hybrids in Nasonia wasps
AU - Werren, John H.
AU - Cohen, Lorna B.
AU - Gadau, Juergen
AU - Ponce, Rita
AU - Baudry, Emmanuelle
AU - Lynch, Jeremy A.
N1 - Funding Information:
We thank Celina Kennedy for head pictures and measurements, Rachel Edwards for assistance in figure preparation, Kevin Chase and Gordon Lark for assistance with EPISTAT, R. Page for collaborations on RAPD mapping in Nasonia, and the Humboldt Foundation for a Feodor Lynen Grant to J. Gadau. We also thank Aisha Siebert and Zichao Yan for assistance, and Nico Posnien for suggesting the use of Congo Red for cuticle imaging. This work was supported by grants to JH Werren ( NSF DEB - 9707665 , NSF DEB 1257053 , and NIH R01 GM70026 ) and by a University of Illinois at Chicago Campus Research Board Pilot Grant ( LYNCH 2013 ) to JAL.
Publisher Copyright:
© 2015 The Authors.
PY - 2016/7/15
Y1 - 2016/7/15
N2 - The animal head is a complex structure where numerous sensory, structural and alimentary structures are concentrated and integrated, and its ontogeny requires precise and delicate interactions among genes, cells, and tissues. Thus, it is perhaps unsurprising that craniofacial abnormalities are among the most common birth defects in people, or that these defects have a complex genetic basis involving interactions among multiple loci. Developmental processes that depend on such epistatic interactions become exponentially more difficult to study in diploid organisms as the number of genes involved increases. Here, we present hybrid haploid males of the wasp species pair Nasonia vitripennis and Nasonia giraulti, which have distinct male head morphologies, as a genetic model of craniofacial development that possesses the genetic advantages of haploidy, along with many powerful genomic tools. Viable, fertile hybrids can be made between the species, and quantitative trail loci related to shape differences have been identified. In addition, a subset of hybrid males show head abnormalities, including clefting at the midline and asymmetries. Crucially, epistatic interactions among multiple loci underlie several developmental differences and defects observed in the F2 hybrid males. Furthermore, we demonstrate an introgression of a chromosomal region from N. giraulti into N. vitripennis that shows an abnormality in relative eye size, which maps to a region containing a major QTL for this trait. Therefore, the genetic sources of head morphology can, in principle, be identified by positional cloning. Thus, Nasonia is well positioned to be a uniquely powerful model invertebrate system with which to probe both development and complex genetics of craniofacial patterning and defects.
AB - The animal head is a complex structure where numerous sensory, structural and alimentary structures are concentrated and integrated, and its ontogeny requires precise and delicate interactions among genes, cells, and tissues. Thus, it is perhaps unsurprising that craniofacial abnormalities are among the most common birth defects in people, or that these defects have a complex genetic basis involving interactions among multiple loci. Developmental processes that depend on such epistatic interactions become exponentially more difficult to study in diploid organisms as the number of genes involved increases. Here, we present hybrid haploid males of the wasp species pair Nasonia vitripennis and Nasonia giraulti, which have distinct male head morphologies, as a genetic model of craniofacial development that possesses the genetic advantages of haploidy, along with many powerful genomic tools. Viable, fertile hybrids can be made between the species, and quantitative trail loci related to shape differences have been identified. In addition, a subset of hybrid males show head abnormalities, including clefting at the midline and asymmetries. Crucially, epistatic interactions among multiple loci underlie several developmental differences and defects observed in the F2 hybrid males. Furthermore, we demonstrate an introgression of a chromosomal region from N. giraulti into N. vitripennis that shows an abnormality in relative eye size, which maps to a region containing a major QTL for this trait. Therefore, the genetic sources of head morphology can, in principle, be identified by positional cloning. Thus, Nasonia is well positioned to be a uniquely powerful model invertebrate system with which to probe both development and complex genetics of craniofacial patterning and defects.
KW - Cleft palette
KW - Craniofacial
KW - Epistasis
KW - Hybrid
KW - Introgression
KW - Nasonia
KW - QTL
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U2 - 10.1016/j.ydbio.2015.12.022
DO - 10.1016/j.ydbio.2015.12.022
M3 - Article
C2 - 26721604
AN - SCOPUS:84951304384
SN - 0012-1606
VL - 415
SP - 391
EP - 405
JO - Developmental Biology
JF - Developmental Biology
IS - 2
ER -