Germ-line chimerism and paternal care in marmosets (Callithrix kuhlii)

C. N. Ross; J. A. French; G. Ortí

doi:10.1073/pnas.0607426104

Edited by John C. Avise, University of California, Irvine, CA, and approved February 14, 2007 (received for review August 25, 2006)

Abstract

The formation of viable genetic chimeras in mammals through the transfer of cells between siblings in utero is rare. Using microsatellite DNA markers, we show here that chimerism in marmoset (Callithrix kuhlii) twins is not limited to blood-derived hematopoietic tissues as was previously described. All somatic tissue types sampled were found to be chimeric. Notably, chimerism was demonstrated to be present in germ-line tissues, an event never before documented as naturally occurring in a primate. In fact, we found that chimeric marmosets often transmit sibling alleles acquired in utero to their own offspring. Thus, an individual that contributes gametes to an offspring is not necessarily the genetic parent of that offspring. The presence of somatic and germ-line chimerism may have influenced the evolution of the extensive paternal and alloparental care system of this taxon. Although the exact mechanisms of sociobiological change associated with chimerism have not been fully explored, we show here that chimerism alters relatedness between twins and may alter the perceived relatedness between family members, thus influencing the allocation of parental care. Consistent with this prediction, we found a significant correlation between paternal care effort and the presence of epithelial chimerism, with males carrying chimeric infants more often than nonchimeric infants. Therefore, we propose that the presence of placental chorionic fusion and the exchange of cell lines between embryos may represent a unique adaptation affecting the evolution of cooperative care in this group of primates.

Footnotes

^†To whom correspondence should be addressed at:
University of Texas Health Science Center, 15355 Lambda Drive, Suite 3.325, South Texas Centers for Biology in Medicine, San Antonio, TX 78245.
E-mail: rossc4{at}uthscsa.edu
Author contributions: C.N.R., J.A.F., and G.O. designed research; C.N.R. performed research; C.N.R. and G.O. analyzed data; and C.N.R., J.A.F., and G.O. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS direct submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0607426104/DC1.
© 2007 by The National Academy of Sciences of the USA