Characterization, Selection, and Trans-Species Polymorphism in the MHC Class II of Heermann’s Gull (Charadriiformes)

Misael Daniel Mancilla-Morales; Enriqueta Velarde; Araceli Contreras-Rodríguez; Zulema Gómez-Lunar; Jesús A. Rosas-Rodríguez; Joseph Heras; José G. Soñanez-Organis; Enrico A. Ruiz

doi:10.3390/genes13050917

Characterization, Selection, and Trans-Species Polymorphism in the MHC Class II of Heermann’s Gull (Charadriiformes)

Misael Daniel Mancilla-Morales^*, Enriqueta Velarde, Araceli Contreras-Rodríguez, Zulema Gómez-Lunar, Jesús A. Rosas-Rodríguez, Joseph Heras, José G. Soñanez-Organis^*, Enrico A. Ruiz^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

The major histocompatibility complex (MHC) enables vertebrates to cope with pathogens and maintain healthy populations, thus making it a unique set of loci for addressing ecology and evolutionary biology questions. The aim of our study was to examine the variability of Heermann’s Gull MHC class II (MHCIIB) and compare these loci with other Charadriiformes. Fifty-nine MHCIIB haplotypes were recovered from sixty-eight Heermann’s Gulls by cloning, of them, twelve were identified as putative true alleles, forty-five as unique alleles, and two as pseudogenes. Intra and interspecific relationships indicated at least two loci in Heermann’s Gull MHCIIB and trans-species polymorphism among Charadriiformes (coinciding with the documented evidence of two ancient avian MHCIIB lineages, except in the Charadriidae family). Additionally, sites under diversifying selection revealed a better match with peptide-binding sites inferred in birds than those described in humans. Despite the negative anthropogenic activity reported on Isla Rasa, Heermann’s Gull showed MHCIIB variability consistent with population expansion, possibly due to a sudden growth following conservation efforts. Duplication must play an essential role in shaping Charadriiformes MHCIIB variability, buffering selective pressures through balancing selection. These findings suggest that MHC copy number and protected islands can contribute to seabird conservation.

Original language	English
Article number	917
Journal	Genes
Volume	13
Issue number	5
DOIs	https://doi.org/10.3390/genes13050917
State	Published - May 2022

Bibliographical note

Funding Information:
Funding: This research was funded by Secretaría de Investigación y Posgrado–Instituto Politécnico Nacional, project numbers 20195761, 20200591, and 20210142 granted to E.A.R.; likewise, by the project number 20210369 granted to Z.G.-L.; by the Universidad de Sonora project number USO513007727 granted to J.G.S.-O. Consejo Nacional de Ciencia y Tecnología (CONACyT) supported the M.D.M.-M. doctoral degree (grant: 630058/577450). Field work in Isla Rasa was funded by the joint fund: Fondo Mexicano para la Conservación de la Naturaleza/Lindblad Expeditions-National Geographic/Packard Foundation.

Funding Information:
This research was funded by Secretaría de Investigación y Posgrado–Instituto Politécnico Nacional, project numbers 20195761, 20200591, and 20210142 granted to E.A.R.; likewise, by the project number 20210369 granted to Z.G.-L.; by the Universidad de Sonora project number USO513007727 granted to J.G.S.-O. Consejo Nacional de Ciencia y Tecnología (CONACyT) supported the M.D.M.-M. doctoral degree (grant: 630058/577450). Field work in Isla Rasa was funded by the joint fund: Fondo Mexicano para la Conservación de la Naturaleza/Lindblad Expeditions-National Geographic/Packard Foundation.Acknowledgments: We thank the personnel of the regional office of Comisión Nacional de Áreas Naturales Protegidas (CONANP) APFF Islas del Golfo de California, Prescott College Kino Bay Center (Lorayne Meltzer), and Secretaría de Marina-Armada de México, for their logistic support and transportation to Isla Rasa, and Andrea Jiménez, of the Laboratorio Nacional de la Biodiversidad at the Institute of Biology, UNAM for technical support. Thanks to the PhD. Andres Aguilar of the Department of Biological Sciences, California State University, Los Angeles, for conceptualization support. Thanks, are also due to Santiago Romero, Alejandra Cano, Angel Soto, Bruno Apodaca, Vanessa Villegas, and UNISON students for their help and assistance in the laboratory work. We appreciate the comments and suggestions of anonymous reviewers.

Publisher Copyright:
© 2022 by the authors. Licensee MDPI, Basel, Switzerland.

Keywords

Gulf of California
Larus heermanni
duplication
peptide-binding sites
seabirds

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10.3390/genes13050917

Cite this

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title = "Characterization, Selection, and Trans-Species Polymorphism in the MHC Class II of Heermann{\textquoteright}s Gull (Charadriiformes)",

abstract = "The major histocompatibility complex (MHC) enables vertebrates to cope with pathogens and maintain healthy populations, thus making it a unique set of loci for addressing ecology and evolutionary biology questions. The aim of our study was to examine the variability of Heermann{\textquoteright}s Gull MHC class II (MHCIIB) and compare these loci with other Charadriiformes. Fifty-nine MHCIIB haplotypes were recovered from sixty-eight Heermann{\textquoteright}s Gulls by cloning, of them, twelve were identified as putative true alleles, forty-five as unique alleles, and two as pseudogenes. Intra and interspecific relationships indicated at least two loci in Heermann{\textquoteright}s Gull MHCIIB and trans-species polymorphism among Charadriiformes (coinciding with the documented evidence of two ancient avian MHCIIB lineages, except in the Charadriidae family). Additionally, sites under diversifying selection revealed a better match with peptide-binding sites inferred in birds than those described in humans. Despite the negative anthropogenic activity reported on Isla Rasa, Heermann{\textquoteright}s Gull showed MHCIIB variability consistent with population expansion, possibly due to a sudden growth following conservation efforts. Duplication must play an essential role in shaping Charadriiformes MHCIIB variability, buffering selective pressures through balancing selection. These findings suggest that MHC copy number and protected islands can contribute to seabird conservation.",

keywords = "Gulf of California, Larus heermanni, duplication, peptide-binding sites, seabirds",

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month = may,

doi = "10.3390/genes13050917",

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T1 - Characterization, Selection, and Trans-Species Polymorphism in the MHC Class II of Heermann’s Gull (Charadriiformes)

AU - Mancilla-Morales, Misael Daniel

AU - Velarde, Enriqueta

AU - Contreras-Rodríguez, Araceli

AU - Gómez-Lunar, Zulema

AU - Rosas-Rodríguez, Jesús A.

AU - Heras, Joseph

AU - Soñanez-Organis, José G.

AU - Ruiz, Enrico A.

PY - 2022/5

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N2 - The major histocompatibility complex (MHC) enables vertebrates to cope with pathogens and maintain healthy populations, thus making it a unique set of loci for addressing ecology and evolutionary biology questions. The aim of our study was to examine the variability of Heermann’s Gull MHC class II (MHCIIB) and compare these loci with other Charadriiformes. Fifty-nine MHCIIB haplotypes were recovered from sixty-eight Heermann’s Gulls by cloning, of them, twelve were identified as putative true alleles, forty-five as unique alleles, and two as pseudogenes. Intra and interspecific relationships indicated at least two loci in Heermann’s Gull MHCIIB and trans-species polymorphism among Charadriiformes (coinciding with the documented evidence of two ancient avian MHCIIB lineages, except in the Charadriidae family). Additionally, sites under diversifying selection revealed a better match with peptide-binding sites inferred in birds than those described in humans. Despite the negative anthropogenic activity reported on Isla Rasa, Heermann’s Gull showed MHCIIB variability consistent with population expansion, possibly due to a sudden growth following conservation efforts. Duplication must play an essential role in shaping Charadriiformes MHCIIB variability, buffering selective pressures through balancing selection. These findings suggest that MHC copy number and protected islands can contribute to seabird conservation.

AB - The major histocompatibility complex (MHC) enables vertebrates to cope with pathogens and maintain healthy populations, thus making it a unique set of loci for addressing ecology and evolutionary biology questions. The aim of our study was to examine the variability of Heermann’s Gull MHC class II (MHCIIB) and compare these loci with other Charadriiformes. Fifty-nine MHCIIB haplotypes were recovered from sixty-eight Heermann’s Gulls by cloning, of them, twelve were identified as putative true alleles, forty-five as unique alleles, and two as pseudogenes. Intra and interspecific relationships indicated at least two loci in Heermann’s Gull MHCIIB and trans-species polymorphism among Charadriiformes (coinciding with the documented evidence of two ancient avian MHCIIB lineages, except in the Charadriidae family). Additionally, sites under diversifying selection revealed a better match with peptide-binding sites inferred in birds than those described in humans. Despite the negative anthropogenic activity reported on Isla Rasa, Heermann’s Gull showed MHCIIB variability consistent with population expansion, possibly due to a sudden growth following conservation efforts. Duplication must play an essential role in shaping Charadriiformes MHCIIB variability, buffering selective pressures through balancing selection. These findings suggest that MHC copy number and protected islands can contribute to seabird conservation.

KW - Gulf of California

KW - Larus heermanni

KW - duplication

KW - peptide-binding sites

KW - seabirds

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DO - 10.3390/genes13050917

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SN - 2073-4425

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JO - Genes

JF - Genes

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ER -

Characterization, Selection, and Trans-Species Polymorphism in the MHC Class II of Heermann’s Gull (Charadriiformes)

Abstract

Bibliographical note

Keywords

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