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Genetic drift vs. natural selection in a long-term small isolated population: major histocompatibility complex class II variation in the Gulf of California endemic porpoise (Phocoena sinus)

Authors

  • ADRIAN MUNGUIA-VEGA,

    1. Centro de Investigaciones Biológicas del Noroeste, SC Mar Bermejo 195, Playa Palo Santa Rita. La Paz, Baja California Sur, México 23090,
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  • YARELI ESQUER-GARRIGOS,

    1. Centro de Investigaciones Biológicas del Noroeste, SC Mar Bermejo 195, Playa Palo Santa Rita. La Paz, Baja California Sur, México 23090,
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  • LORENZO ROJAS-BRACHO,

    1. Programa Nacional de Mamíferos Marinos, Instituto Nacional de Ecología/Centro de Investigación Científica y Educación Superior de Ensenada, Km. 107, Carretera Ensenada–Tijuana, Ensenada, Baja California, México 22860,
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  • RICARDO VAZQUEZ-JUAREZ,

    1. Centro de Investigaciones Biológicas del Noroeste, SC Mar Bermejo 195, Playa Palo Santa Rita. La Paz, Baja California Sur, México 23090,
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  • AINES CASTRO-PRIETO,

    1. Centro de Investigación Científica y Educación Superior de Ensenada, Km. 107, Carretera Ensenada–Tijuana. Ensenada, Baja California, México 22860
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  • SERGIO FLORES-RAMIREZ

    1. Laboratorio de Ecología Molecular y Genética de la Conservación, Universidad Autónoma de Baja California Sur, Km. 4.5 Carretera La Paz–Los Cabos, La Paz, Baja California Sur, México 23080,
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correspondence: Adrian Munguia-vega, School of Natural Resources, University of Arizona, Tucson, AZ 85721, USA. Fax: (520) 621 8801, E-mail: airdrian@email.arizona.edu

Abstract

Although many studies confirm long-term small isolated populations (e.g. island endemics) commonly sustain low neutral genetic variation as a result of genetic drift, it is less clear how selection on adaptive or detrimental genes interplay with random forces. We investigated sequence variation at two major histocompatibility complex (Mhc) class II loci on a porpoise endemic to the upper Gulf of California, México (Phocoena sinus, or vaquita). Its unique declining population is estimated around 500 individuals. Single-strand conformation polymorphism analysis revealed one putative functional allele fixed at the locus DQB (n = 25). At the DRB locus, we found two presumed functional alleles (n = 29), differing by a single nonsynonymous nucleotide substitution that could increase the stability at the dimer interface of αβ-heterodimers on heterozygous individuals. Identical trans-specific DQB1 and DRB1 alleles were identified between P. sinus and its closest relative, the Burmeister's porpoise (Phocoena spinipinnis). Comparison with studies on four island endemic mammals suggests fixation of one allele, due to genetic drift, commonly occurs at the DQA or DQB loci (effectively neutral). Similarly, deleterious alleles of small effect are also effectively neutral and can become fixed; a high frequency of anatomical malformations on vaquita gave empirical support to this prediction. In contrast, retention of low but functional polymorphism at the DRB locus was consistent with higher selection intensity. These observations indicated natural selection could maintain (and likely also purge) some crucial alleles even in the face of strong and prolonged genetic drift and inbreeding, suggesting long-term small populations should display low inbreeding depression. Low levels of Mhc variation warn about a high susceptibility to novel pathogens and diseases in vaquita.

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