Professor of Biological Sciences and
Adjunct Professor of Human Genetics
A.B. University of California, Berkeley
Ph.D. Harvard University
Michael Shapiro's Lab Page
Michael Shapiro's PubMed Literature Search
Molecular Biology Program
Evolutionary Genetics, Genomics, and Developmental Biology
Despite our longstanding interest in how animals acquire novel morphological and behavioral characteristics, we know remarkably little about the number, location, and types of mutations that control phenotypic change. We are exploiting the remarkable diversity among domestic pigeons by pioneering developmental, genetic, and genomic approaches to determine the molecular and mechanistic bases of variation. As a result of our efforts over the past few years, we have discovered genomic and developmental changes controlling differences in feather architecture (Shapiro et al., 2013; Domyan et al., 2016) and color (Guernsey et al., 2013; Domyan et al., 2014), including traits with direct relevance to diversity and disease beyond pigeons. For example, the specific genes that we implicated in plumage color phenotypes in pigeons also contribute to both natural pigmentation diversity and skin disease in humans, including melanoma risk. Moreover, the same gene that is associated with a major change in feather growth underlies convergent evolution of an analogous trait in another bird species (Vickrey et al., 2015). Thus, by elucidating the complex interactions among genes that control variation in pigeons, we also enrich our mechanistic understanding of adaptive and nonadaptive variation across species.
A compelling experimental model for understanding variation in vertebrates
We have entered an exciting period in the biomedical sciences. Instead of relying exclusively on a small group of traditional model organisms, we can now select appropriate animal models for studying specific traits and processes based upon their biology rather than historical precedence. In The Origin of Species, Charles Darwin enthusiastically promotes the enormous diversity among domestic pigeons — generated by thousands of years of artificial selection on a single species by human breeders — as an important proxy for understanding natural selection in wild populations and species. Ever since Neolithic times, pigeon breeders have selected for dramatic differences in morphological and behavioral traits such as skeletal morphology, feather ornaments, vocalizations, colors, and color patterns in over 350 breeds. The number and stunning magnitude of differences among breeds are often more characteristic of macroevolutionary changes than of variation within a single species (see Stringham et al. 2012, Shapiro and Domyan 2013). However, because all breeds belong to the same species, we can use traditional genetic crosses and whole-genome resequencing to map the genes and mutations that control this striking variation.
A novel entry point to general mechanisms of variation
Our studies of pigeons illustrate how combining comparative genomics and population-based analyses can lead directly to discovering the genetic and developmental basis of variation. Many of the traits that vary among pigeon breeds also vary among wild species of birds and other animals; thus, the pigeon is a compelling model for identifying the genetic basis of variation in traits of general evolutionary significance. Moreover, variation in many traits in domestic pigeons (e.g., head crests, feathered feet, beak elaboration) is constructive rather than regressive: Breeds derived from the ancestral rock pigeon possess traits that the ancestor does not have. Although regressive (loss and reduction) traits are important, the genetic basis of constructive traits in vertebrates remains comparatively poorly understood. Collectively, our complementary genetic, genomic, and developmental approaches are enabling us to identify the molecular basis of the astonishing variation among pigeons, thereby opening new avenues to understand the potential roles of specific genes in variation among vertebrates in general.
A.I. Vickrey, R. Bruders, Z. Kronenberg, E. Mackey, R.J. Bohlender, E. Maclary, R. Maynez, E.J. Osborne, K.P. Johnson, C.D. Huff, M. Yandell, M.D. Shapiro. (2018) Introgression of regulatory alleles and a missense coding mutation drive plumage pattern diversity in the rock pigeon. eLife 7: e34803.
C. Holt, M. Campbell, D.A. Keays, N. Edelman, A. Kapusta, E. Maclary, E. Domyan, A. Suh, W.C. Warren, M. Yandell, M.T.P. Gilbert, M.D. Shapiro. (2018) Improved genome assembly and annotation for the rock pigeon (Columba livia). G3: Genes | Genomes | Genetics 8: 1391-1398.
E.T. Domyan, M.D. Shapiro. (2017) Pigeonetics takes flight: Evolution, development, and genetics of intraspecific variation. Developmental Biology 427: 241-250.
E.F. Boer, H.F. Van Hollebecke, M.D. Shapiro. (2017) Genomic determinants of epidermal appendage patterning and structure in domestic birds. Developmental Biology. doi: 10.1016/j.ydbio.2017.03.022.
- E.T. Domyan, Z. Kronenberg, C. Infante, A.I. Vickrey, S.A. Stringham, R. Bruders, M.W. Guernsey, S. Park, J. Payne, R. Beckstead, G. Kardon, D.B. Menke, M. Yandell, M.D. Shapiro. (2016) Molecular shifts in limb identity underlie development of feathered feet in two domestic avian species. eLife 5: e12115
- Z. Kronenberg, E.J. Osborne, K. Cone, E. Domyan, M.D. Shapiro, N. Elde, M, Yandell. (2015) Wham: Identifying Structural Variants of Biological Consequence. PLoS Computational Biology 11: e1004572
- A.I. Vickrey, E.T. Domyan, M.P. Horvath, M.D. Shapiro. (2015) Convergent evolution of head crests in two domesticated columbids is associated with different missense mutations in EphB2. Molecular Biology and Evolution 32: 2657-64
- S.A. Stringham, M.D. Shapiro. (2015) Microevolution and the genetic basis of vertebrate diversity: examples from teleost fishes. In K.P. Dial, N.H. Shubin, E.L. Brainerd (eds.), Great Transformations in Vertebrate Evolution. University of Chicago Press, Chicago.
- E.T. Domyan, M.W. Guernsey, Z. Kronenberg, S. Krishnan, R.E. Boissy, A. Vickrey, C. Rodgers, P. Cassidy, S.A. Leachman, J.W. Fondon III, M. Yandell, M.D. Shapiro. (2014) Epistatic and combinatorial effects of pigmentary gene mutations in the domestic pigeon. Current Biology 24: 459-464
- C.T. Miller, A.M. Glazer, B.R. Summers, B.K. Blackman, A.R. Norman, M.D. Shapiro, B.L. Cole, C.L. Peichel, D. Schluter, D.M. Kingsley. (2014) Additive and clustered quantitative trait loci control anatomically regional skeletal evolution in sticklebacks. Genetics 197: 405-420
- M.W. Guernsey, L. Ritscher, M.A. Miller, T. Shoeneberg, M.D. Shapiro. (2013) A Val85Met mutation in melanocortin-1 receptor is associated with reductions in eumelanic pigmentation and cell surface expression in domestic rock pigeons (Columba livia). PLoS ONE 8: e74475
- M.D. Shapiro*, Z. Kronenberg, C. Li, E.T. Domyan, H. Pan, M. Campbell, H. Tan, C.D. Huff, Haofu Hu, A.I. Vickrey, S.A. Nielsen, S.A. Stringham, Hao Hu, E. Willerslev, M.T.P. Gilbert, M. Yandell, G. Zhang, J. Wang* (* co-corresponding and senior authors). (2013) Genomic diversity and evolution of the head crest in the rock pigeon. Science 339: 1063-1067
- M.D. Shapiro and E.T. Domyan. (2013) Quick Guide: Domestic Pigeons. Current Biology 23: R302-303
- S.A. Stringham, E.A. Mulroy, J. Xing, D. Record, M.W. Guernsey, J.T. Aldenhoven, E.J. Osborne, M.D. Shapiro. (2012) Divergence, convergence, and the ancestry of feral populations in the domestic rock pigeon. Current Biology 22: 302-308 (Cover article)
- T.A. Castoe, A.M. Bronikowski, E.D. Brodie III, S.V. Edwards, M.E. Pfrender, M.D. Shapiro, D.D. Pollock, W.C. Warren. (2011) A proposal to sequence the genome of a garter snake (Thamnophis sirtalis). Standards in Genomic Sciences 4: 257-270
- J.T. Aldenhoven, M.A. Miller, P. Showers Corneli, M.D. Shapiro. (2010) Phylogeography of ninespine sticklebacks (Pungitius pungitius) in North America: glacial refugia and the origins of adaptive traits. Molecular Ecology 19: 4061-4076
- Y.F. Chan, M.E. Marks, F.C. Jones, G. Villarreal Jr, M.D. Shapiro, S. Fisher, A.M. Southwick, D.M. Absher, J. Grimwood, J. Schmutz, R.M. Myers, D. Petrov, B. Jónsson, D. Schluter, M.A. Bell, D.M. Kingsley. (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 5963: 302-305
- M.D. Shapiro, B.R. Summers, S. Balabhadra, J.T. Aldenhoven, A.L. Miller, C. Cunningham, M.A. Bell, D.M. Kingsley. (2009) The genetic architecture of skeletal convergence and sex determination in ninespine sticklebacks. Current Biology 19: 1140-1145
- J.A. Ross, J.R. Urton, J. Boland, M.D. Shapiro, C.L. Peichel. (2009) Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae). PLoS Genetics 5: e1000391
- M.D. Shapiro, N.H. Shubin, J.P. Downs. (2007) Limb reduction and diversity in reptilian evolution, pp. 225-244. In B.K. Hall (ed.), Fins Into Limbs: Evolution, Development, and Transformation, University of Chicago Press
- M.D. Shapiro, M.A. Bell, D.M. Kingsley. (2006) Parallel genetic origins of pelvic reduction in vertebrates. Proc Natl Acad Sci USA 103: 13753-13718
- M.D. Shapiro, M.E. Marks, C.L. Peichel, B.K. Blackman, K.S. Nereng, B. Jonsson, D. Schluter, D.M. Kingsley. (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428: 717-723
- P.F. Colosimo, C.L. Peichel, K. Nereng, B.K. Blackman, M.D. Shapiro, D. Schluter, D.M. Kingsley. (2004) The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS-Biology 2: 635-641
- M.D. Shapiro, J. Hanken, N. Rosenthal. (2003) Developmental basis of evolutionary digit loss in the Australian lizard Hemiergis. J Exp Zool 297B: 48-56
- M.D. Shapiro. (2002) Developmental morphology of limb reduction in Hemiergis (Squamata: Scincidae): chondrogenesis, osteogenesis, and heterochrony. Journal of Morphology 254: 211-231 (Cover article)
- M.D. Shapiro, T.F. Carl. (2001) Novel features of tetrapod limb development in two non-traditional model species: a skink and a direct-developing frog, pp. 337-361. In M. Zelditch (ed.), Beyond Heterochrony: The Evolution of Development. New York: Wiley-Liss. (Cover photo)
- J. Xavier-Neto, M.D. Shapiro, L. Houghton, N. Rosenthal. (2000) Sequential programs of retinoic acid synthesis in the myocardial and epicardial layers of the developing avian heart. Developmental Biology 219: 129-141