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Evolution of Suiform Aromatases: Ancestral Duplication with Conservation of Tissue-Specific Expression in the Collared Peccary (Pecari tayassu)

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Abstract

Aromatase cytochrome P450 (P450arom), the enzyme that catalyzes estrogen synthesis, is required for successful reproduction and is encoded by a single copy gene (CYP19) in most mammals. However, pigs and their distant suiform relatives the peccaries experienced CYP19 duplication. Here, the evolutionary origin of CYP19 duplication, and the evolution of the gene paralogs, was explored further in collared peccaries (Pecari tayassu). Exons IV and V, and the intervening intron, representing duplicated CYP19 genes, were cloned and sequenced from collared peccary, pig, and hippopotamus. Sequence alignment and analysis identified a gene conversion in collared peccary with a breakpoint 102 base pairs (bp) upstream of exon V. Phylogenetic analyses of nucleotide and amino acid sequence upstream of the breakpoint supported a tree in which one peccary sequence was orthologous with the porcine gonadal gene. Cloning and sequencing of tissue transcripts, using reverse-transcriptase polymerase chain reaction techniques (RT-PCR), confirmed that the gonadal ortholog was expressed in collared peccary testis. Orthology of the other genomic sequence with the porcine placental gene was not resolved, but its placenta-specific expression in collared peccary was confirmed by similar transcript analysis. Immunoblot and enzyme activity in collared peccary testes demonstrated much lower levels of P450arom than in pig testis. Collared peccary placental P450arom expression also seemed much lower than pigs. Thus, suiform CYP19 genes arose from an ancestral duplication that has maintained gonad- and placenta-specific expression, but at lower levels in peccaries than pigs, perhaps facilitating the emergence of different reproductive strategies as Suiformes diverged and evolved.

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Acknowledgments

The authors express thanks to Dr. Oliver Ryder and Leona Chemnick, Center for Reproduction of Endangered Species, San Diego Zoo, San Diego CA for their gift of genomic DNA samples, and to the staff at UFERSA, Mossoró for care of the animals in the captive colony of collared peccaries.

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Authors and Affiliations

  1. Department of Population Health and Reproduction, University of California, Davis, CA, USA

    C. J. Corbin & A. J. Conley

  2. Department of Biological Sciences, University of South Carolina, Columbia, SC, USA

    A. L. Hughes

  3. Arizona Game and Fish Department, Tucson, AZ, USA

    J. R. Heffelfinger

  4. Department of Animal Science, University of California, Davis, CA, USA

    T. Berger & J. F. Roser

  5. Department of Medicine and Epidemiology, University of California, Davis, CA, USA

    T. B. Waltzek

  6. Faculdade de Medicina Veterinária e Zootecnia, University of São Paulo, São Paulo, Brazil

    T. C. Santos & M. A. Miglino

  7. Universidade Federal do Semi-Árido, Mossoró, Brazil

    M. F. Oliveira

  8. Faculdade de Zootecnia e Engenharia de Alimentos, University of São Paulo, Pirassununga, Brazil

    F. C. Braga & F. V. Meirelles

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  1. C. J. Corbin
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  2. A. L. Hughes
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  3. J. R. Heffelfinger
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  4. T. Berger
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  5. T. B. Waltzek
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  6. J. F. Roser
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  7. T. C. Santos
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  8. M. A. Miglino
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  9. M. F. Oliveira
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  10. F. C. Braga
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  11. F. V. Meirelles
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  12. A. J. Conley
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Correspondence to A. J. Conley.

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Corbin, C.J., Hughes, A.L., Heffelfinger, J.R. et al. Evolution of Suiform Aromatases: Ancestral Duplication with Conservation of Tissue-Specific Expression in the Collared Peccary (Pecari tayassu). J Mol Evol 65, 403–412 (2007). https://doi.org/10.1007/s00239-007-9021-0

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  • DOI: https://doi.org/10.1007/s00239-007-9021-0

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