Transcriptomic insights into the genetic basis of mammalian limb diversity.
From bat wings to whale flippers, limb diversification has been crucial to the evolutionary success of mammals. We performed the first transcriptome-wide study of limb development in multiple species to explore the hypothesis that mammalian limb diversification has proceeded through the differential expression of conserved shared genes, rather than by major changes to limb patterning. Specifically, we investigated the manner in which the expression of shared genes has evolved within and among mammalian species.



We assembled and compared transcriptomes of bat, mouse, opossum, and pig fore- and hind limbs at the ridge, bud, and paddle stages of development. Results suggest that gene expression patterns exhibit larger variation among species during later than earlier stages of limb development, while within species results are more mixed. Consistent with the former, results also suggest that genes expressed at later developmental stages tend to have a younger evolutionary age than genes expressed at earlier stages. A suite of key limb-patterning genes was identified as being differentially expressed among the homologous limbs of all species. However, only a small subset of shared genes is differentially expressed in the fore- and hind limbs of all examined species. Similarly, a small subset of shared genes is differentially expressed within the fore- and hind limb of a single species and among the forelimbs of different species.



Taken together, results of this study do not support the existence of a phylotypic period of limb development ending at chondrogenesis, but do support the hypothesis that the hierarchical nature of development translates into increasing variation among species as development progresses.
School of Integrative Biology, University of Illinois, 505 S Goodwin Avenue, Urbana, IL, 61801, USA.
Jennifer A
JA
Maier
Department of Bioengineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093, USA.
Marcelo
M
Rivas-Astroza
Department of Genetics, University of Texas MD Anderson Cancer Center, 1515 Holcombe Boulevard, Houston, TX, 77030, USA.
Jenny
J
Deng
School of Integrative Biology, University of Illinois, 505 S Goodwin Avenue, Urbana, IL, 61801, USA.
Anna
A
Dowling
School of Integrative Biology, University of Illinois, 505 S Goodwin Avenue, Urbana, IL, 61801, USA.
Paige
P
Oboikovitz
Department of Bioengineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093, USA.
Xiaoyi
X
Cao
Department of Genetics, University of Texas MD Anderson Cancer Center, 1515 Holcombe Boulevard, Houston, TX, 77030, USA.
Richard R
RR
Behringer
Department of Biological Sciences, Idaho State University, 921 South 8th Avenue, Pocatello, ID, 83209, USA.
Chris J
CJ
Cretekos
Department of Obstetrics and Gynecology, State University Downstate Medical Center, 450 Clarkson, Avenue, Brooklyn, NY, 11203, USA.
John J
JJ
Rasweiler
Department of Bioengineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093, USA.
Sheng
S
Zhong
School of Integrative Biology, University of Illinois, 505 S Goodwin Avenue, Urbana, IL, 61801, USA. ksears@life.illinois.edu.|Institute for Genomic Biology, University of Illinois, 1206 W Gregory Drive, Urbana, IL, 61801, USA. ksears@life.illinois.edu.
Karen E
KE
Sears
D000818:Animals; D005075:Biological Evolution; D005121:Extremities / Q000033:anatomy & histology / Q000254:growth & development / Q000502:physiology; D018507:Gene Expression Regulation, Developmental; D008322:Mammals / Q000033:anatomy & histology / Q000145:classification* / Q000235:genetics* / Q000254:growth & development; D059467:Transcriptome; D014921:Wings, Animal
Bat; Differential expression; Diversification; Limb; Mammalian; Mouse; Opossum; Pig; Transcriptome