Heterotaxy in Caenorhabditis: widespread natural variation in left-right arrangement of the major organs.
Although the arrangement of internal organs in most metazoans is profoundly left-right (L/R) asymmetric with a predominant handedness, rare individuals show full (mirror-symmetric) or partial (heterotaxy) reversals. While the nematode Caenorhabditis elegans is known for its highly determinate development, including stereotyped L/R organ handedness, we found that L/R asymmetry of the major organs, the gut and gonad, varies among natural isolates of the species in both males and hermaphrodites. In hermaphrodites, heterotaxy can involve one or both bilaterally asymmetric gonad arms. Male heterotaxy is probably not attributable to relaxed selection in this hermaphroditic species, as it is also seen in gonochoristic Caenorhabditis species. Heterotaxy increases in many isolates at elevated temperature, with one showing a pregastrulation temperature-sensitive period, suggesting a very early embryonic or germline effect on this much later developmental outcome. A genome-wide association study of 100 isolates showed that male heterotaxy is associated with three genomic regions. Analysis of recombinant inbred lines suggests that a small number of loci are responsible for the observed variation. These findings reveal that heterotaxy is a widely varying quantitative trait in an animal with an otherwise highly stereotyped anatomy, demonstrating unexpected plasticity in an L/R arrangement of the major organs even in a simple animal.This article is part of the themed issue 'Provocative questions in left-right asymmetry'.
Department of MCD Biology and Neuroscience Research Institute, University of California, Santa Barbara, CA 93106, USA.
Melissa R
0000-0001-6284-3255
MR
Alcorn
Department of MCD Biology and Neuroscience Research Institute, University of California, Santa Barbara, CA 93106, USA.
Davon C
DC
Callander
School of Biological Sciences, University of Auckland, Auckland, New Zealand.
Agustín
A
López-Santos
Department of MCD Biology and Neuroscience Research Institute, University of California, Santa Barbara, CA 93106, USA.|School of Biological Sciences, University of Auckland, Auckland, New Zealand.
Yamila N
YN
Torres Cleuren
Department of MCD Biology and Neuroscience Research Institute, University of California, Santa Barbara, CA 93106, USA.|Department of MCD Biology, University of Colorado, Boulder, CO 80309-0347, USA.
Bilge
0000-0003-4337-4582
B
Birsoy
Department of MCD Biology and Neuroscience Research Institute, University of California, Santa Barbara, CA 93106, USA.
Pradeep M
0000-0002-4220-0559
PM
Joshi
School of Biological Sciences, University of Auckland, Auckland, New Zealand.
Anna W
AW
Santure
Department of MCD Biology and Neuroscience Research Institute, University of California, Santa Barbara, CA 93106, USA joel.rothman@lifesci.ucsb.edu.|School of Biological Sciences, University of Auckland, Auckland, New Zealand.
Joel H
0000-0002-6844-1377
JH
Rothman
D000818:Animals; D019521:Body Patterning; D017173:Caenorhabditis elegans / Q000196:embryology* / Q000235:genetics*; D041981:Gastrointestinal Tract / Q000196:embryology; D055106:Genome-Wide Association Study; D006066:Gonads / Q000196:embryology; D008297:Male; D038081:Organogenesis
C. elegans; GWAS; heterotaxy; left–right asymmetry; natural variation