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Trans-species polymorphism and evidence of selection on class II MHC loci in tuco-tucos (Rodentia: Ctenomyidae)

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Abstract

Balancing selection acting over the evolutionary history of a lineage can result in the retention of alleles among species for longer than expected under neutral evolution. The associated pattern of trans-species polymorphism, in which similar or even identical alleles are shared among species, is often used to infer that balancing selection has occurred. The genes of the major histocompatibility complex (MHC) are thought to be subject to balancing selection that maintains alleles associated with response to specific pathogens. To explore the role of balancing selection in shaping MHC diversity in ctenomyid rodents, we examined allelic variability at the class II DRB and DQA loci in 18 species in the genus Ctenomys. Previous studies of four of these species had revealed significant within-population evidence of positive selection on MHC loci. The current study expands upon these analyses to (1) evaluate among-species evidence of positive selection and (2) explore the potential for balancing selection on MHC genes. Interspecific nucleotide sequence variation revealed significant evidence of positive selection on the DRB and DQA loci. At the same time, comparisons of phylogenetic trees for these MHC loci with a putative species tree based on mitochondrial sequence data revealed multiple examples of trans-specific polymorphism, including sharing of identical DRB and DQA alleles among distantly related species of Ctenomys. These findings suggest that MHC genes in these animals have historically been subject to balancing selection and yield new insights into the complex suite of forces shaping MHC diversity in free-living vertebrates.

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Acknowledgment

We thank David Vieites for his invaluable assistance with the phylogenetic analyses and Enrique Lessa and two anonymous reviewers for insightful comments on previous versions of this manuscript. We particularly wish to thank Tina Hambuch for her pioneering studies of MHC variation in ctenomyids. Financial support was provided by the Universidad Nacional de Mar del Plata, the Agencia de Promoción Científica y Tecnológica (FONCYT-PICT 01–09846), the National Science Foundation (DEB-9704462 and DEB-0128857), and CONICET (Beca Doctoral Mixta to APC). All field procedures conformed to guidelines of the American Society of Mammalogists for the capture, handling, and care of mammals (Animal Care and Use Committee 1998).

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  1. Laboratorio de Ecofisiología, Departamento de Biología, Universidad Nacional de Mar del Plata, C.C. 1245, Mar del Plata, Argentina

    Ana Paula Cutrera

  2. Museum of Vertebrate Zoology, University of California at Berkeley, Berkeley, CA, 94720-3160, USA

    Eileen A. Lacey

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  1. Ana Paula Cutrera
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Correspondence to Ana Paula Cutrera.

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Cutrera, A.P., Lacey, E.A. Trans-species polymorphism and evidence of selection on class II MHC loci in tuco-tucos (Rodentia: Ctenomyidae). Immunogenetics 59, 937–948 (2007). https://doi.org/10.1007/s00251-007-0261-3

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