Colonizing the world in spite of reduced MHC variation

LAURA GANGOSO; MIGUEL ALCAIDE; JUAN MANUEL GRANDE; JOAQUÍN MUÑOZ; S. L. TALBOT; A. SONSTHAGEN; G. K. SAGE; FIGUEROLA, J.

JOURNAL OF EVOLUTIONARY BIOLOGY

WILEY-BLACKWELL PUBLISHING, INC

Año: 2012 vol. 25 p. 1438 - 1447

1010-061X

The Major Histocompatibility Complex (MHC), which harbours the most polymorphic vertebrate genes, is known to play a critical role during the host-pathogen coevolutionary arms race. However, the extent to which MHC diversity determines disease susceptibility and long-term persistence of populations is currently under debate, as recent studies have demonstrated that low MHC variability does not necessarily hamper population viability. However, these studies typically assayed small and decimated populations in species with restricted distribution, thereby making inferences about the evolutionary potential of these populations difficult. Here, we show that MHC impoverishment has not constrained the ecological radiation and flourishing of falcons (Aves: Falconidae) worldwide. We found two remarkably different patterns of MHC variation within the genus Falco. While MHC variation in kestrels (the most basal group within the genus) is very high, falcons exhibit ancestrally low intra- and inter-specific MHC variability. This pattern does not appear to be due to the inadvertent survey of paralogous genes. Transcription evidence from the spleen, coupled with evidence based on neutral variation, support neither an explanation based on pseudogenization, nor the effect of genetic drift. We propose the falcons went through an evolutionary transition, driven and maintained by natural selection, from primarily highly variable towards low polymorphic and slow evolving MHC genes with a very specific immune function. This study highlights that the importance of MHC diversity cannot be generalized among vertebrates and hints the evolution of compensatory immune mechanisms in falcons to cope with emerging and continuously evolving pathogens.