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Open Access Highly Accessed Research article

Molecular adaptation of telomere associated genes in mammals

Claire C Morgan12, Ann M Mc Cartney12, Mark TA Donoghue34, Noeleen B Loughran5, Charles Spillane3, Emma C Teeling6 and Mary J O’Connell127*

Author Affiliations

1 Bioinformatics and Molecular Evolution Group, School of Biotechnology, Dublin City University, Glasnevin, Dublin 9, Ireland

2 Centre for Scientific Computing & Complex Systems Modelling (SCI-SYM), Dublin City University, Glasnevin, Dublin 9, Ireland

3 Genetics and Biotechnology Lab, Plant and AgriBiosciences Research Centre, National University of Ireland Galway (NUIG), Aras de Brun C306, Galway, Ireland

4 Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA

5 Program in Molecular Structure and Function, Hospital for Sick Children, Toronto, Canada and Departments of Biochemistry and Molecular Genetics, University of Toronto, Toronto, Canada

6 School of Biology and Environmental Science & UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Belfield, Dublin 4, Ireland

7 Current address: Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA

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BMC Evolutionary Biology 2013, 13:251  doi:10.1186/1471-2148-13-251

Published: 15 November 2013

Abstract

Background

Placental mammals display a huge range of life history traits, including size, longevity, metabolic rate and germ line generation time. Although a number of general trends have been proposed between these traits, there are exceptions that warrant further investigation. Species such as naked mole rat, human and certain bat species all exhibit extreme longevity with respect to body size. It has long been established that telomeres and telomere maintenance have a clear role in ageing but it has not yet been established whether there is evidence for adaptation in telomere maintenance proteins that could account for increased longevity in these species.

Results

Here we carry out a molecular investigation of selective pressure variation, specifically focusing on telomere associated genes across placental mammals. In general we observe a large number of instances of positive selection acting on telomere genes. Although these signatures of selection overall are not significantly correlated with either longevity or body size we do identify positive selection in the microbat species Myotis lucifugus in functionally important regions of the telomere maintenance genes DKC1 and TERT, and in naked mole rat in the DNA repair gene BRCA1.

Conclusion

These results demonstrate the multifarious selective pressures acting across the mammal phylogeny driving lineage-specific adaptations of telomere associated genes. Our results show that regardless of the longevity of a species, these proteins have evolved under positive selection thereby removing increased longevity as the single selective force driving this rapid rate of evolution. However, evidence of molecular adaptations specific to naked mole rat and Myotis lucifugus highlight functionally significant regions in genes that may alter the way in which telomeres are regulated and maintained in these longer-lived species.

Keywords:
Positive selection; Mammal molecular evolution; Telomere; Senescence; Longevity