Adaptive and neutral genetic differentiation among Scottish and endangered Irish red grouse (Lagopus lagopus scotica)

Yvonne Meyer-Lucht; Kevin P. Mulder; Marianne C. James; Barry J. McMahon; Kieran Buckley; Stuart B. Piertney; Jacob Höglund

doi:10.1007/s10592-016-0810-0

Adaptive and neutral genetic differentiation among Scottish and endangered Irish red grouse (Lagopus lagopus scotica)

Yvonne Meyer-Lucht^*, Kevin P. Mulder, Marianne C. James, Barry J. McMahon, Kieran Buckley, Stuart B. Piertney, Jacob Höglund

^*Corresponding author for this work

Aberdeen Centre For Environmental Sustainability

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

18 Citations (Scopus)

Abstract

Studying patterns of intra-specific genetic variation among populations allows for a better understanding of population structure and local adaptation. However, those patterns may differ according to the genetic markers applied, as neutral genetic markers reflect demographic processes and random genetic drift, whereas adaptive markers also carry the footprint of selection. In combination, neutral and adaptive genetic markers permit to assess the relative roles of drift and selection in shaping population structure. Among the best understood adaptive genetic loci are the genes of the major histocompatibility complex (MHC). We here study variation and differentiation at neutral SNP markers and MHC class II genes in red grouse (Lagopus lagopus scotica) from Ireland and Scotland. Irish red grouse populations are fragmented and drastically declining, but red grouse are abundant in Scotland. We find evidence for positive selection acting on the MHC genes and variation in MHC gene copy numbers among Irish individuals. Furthermore, there was significant population differentiation among red grouse from Ireland and Scotland at the neutral SNP markers (F_ST = 0.084) and the MHC-BLB genes (F_ST: BLB1 = 0.116, BLB2 = 0.090, BLB3 = 0.104). Differentiation at the MHC-BLB1 was significantly higher than at the neutral SNP markers, suggesting that selection plays an important role in shaping MHC variation, in addition to genetic drift. We speculate that the observed differentiation pattern might be due to local adaptation to different parasite regimes. These findings have strong conservation implications and we advise against the introduction of Scottish red grouse to supplement Irish populations.

Original language	English
Pages (from-to)	615-630
Number of pages	16
Journal	Conservation Genetics
Volume	17
Issue number	3
Early online date	21 Jan 2016
DOIs	https://doi.org/10.1007/s10592-016-0810-0
Publication status	Published - Jun 2016

Bibliographical note

Acknowledgements: We are very thankful to Ahmed Sayadi for
helping with the resampling procedures, to Gunilla Engstro¨m for
support in the genetic lab, and to Magnus Johansson for helpful
discussions. Moreover, we thank the four anonymous reviewers for helpful and constructive advice on this manuscript. Irish feather samples were collected all over Ireland by volunteers from the Irish Grey Partridge Conservation Trust, the National Association of Regional Games Councils of Ireland, the Irish National Park and Wildlife Service, BirdWatch Ireland and red grouse enthusiasts from the Republic of Ireland. We thank staff at the NERC Biomolecular Analysis Facility at Sheffield for SNP genotyping.

This study was funded by the Carl Tryggers foundation, the Erasmus Mundus master program in Evolutionary Biology (MEME), the Helge Ax:son Johnson foundation, the Native Species Conservation Committee of Dublin Zoo, Fota Wildlife Park, the UK Natural Environment Research Council and the Swedish Research Council.

Keywords

Galliformes
Genetic drift
Local adaptation
Major histocompatibility complex
MHC BLB exon 2
Single locus amplification

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title = "Adaptive and neutral genetic differentiation among Scottish and endangered Irish red grouse (Lagopus lagopus scotica)",

abstract = "Studying patterns of intra-specific genetic variation among populations allows for a better understanding of population structure and local adaptation. However, those patterns may differ according to the genetic markers applied, as neutral genetic markers reflect demographic processes and random genetic drift, whereas adaptive markers also carry the footprint of selection. In combination, neutral and adaptive genetic markers permit to assess the relative roles of drift and selection in shaping population structure. Among the best understood adaptive genetic loci are the genes of the major histocompatibility complex (MHC). We here study variation and differentiation at neutral SNP markers and MHC class II genes in red grouse (Lagopus lagopus scotica) from Ireland and Scotland. Irish red grouse populations are fragmented and drastically declining, but red grouse are abundant in Scotland. We find evidence for positive selection acting on the MHC genes and variation in MHC gene copy numbers among Irish individuals. Furthermore, there was significant population differentiation among red grouse from Ireland and Scotland at the neutral SNP markers (FST = 0.084) and the MHC-BLB genes (FST: BLB1 = 0.116, BLB2 = 0.090, BLB3 = 0.104). Differentiation at the MHC-BLB1 was significantly higher than at the neutral SNP markers, suggesting that selection plays an important role in shaping MHC variation, in addition to genetic drift. We speculate that the observed differentiation pattern might be due to local adaptation to different parasite regimes. These findings have strong conservation implications and we advise against the introduction of Scottish red grouse to supplement Irish populations.",

keywords = "Galliformes, Genetic drift, Local adaptation, Major histocompatibility complex, MHC BLB exon 2, Single locus amplification",

author = "Yvonne Meyer-Lucht and Mulder, {Kevin P.} and James, {Marianne C.} and McMahon, {Barry J.} and Kieran Buckley and Piertney, {Stuart B.} and Jacob H{\"o}glund",

note = "Acknowledgements: We are very thankful to Ahmed Sayadi for helping with the resampling procedures, to Gunilla Engstro¨m for support in the genetic lab, and to Magnus Johansson for helpful discussions. Moreover, we thank the four anonymous reviewers for helpful and constructive advice on this manuscript. Irish feather samples were collected all over Ireland by volunteers from the Irish Grey Partridge Conservation Trust, the National Association of Regional Games Councils of Ireland, the Irish National Park and Wildlife Service, BirdWatch Ireland and red grouse enthusiasts from the Republic of Ireland. We thank staff at the NERC Biomolecular Analysis Facility at Sheffield for SNP genotyping. This study was funded by the Carl Tryggers foundation, the Erasmus Mundus master program in Evolutionary Biology (MEME), the Helge Ax:son Johnson foundation, the Native Species Conservation Committee of Dublin Zoo, Fota Wildlife Park, the UK Natural Environment Research Council and the Swedish Research Council.",

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AU - Meyer-Lucht, Yvonne

AU - Mulder, Kevin P.

AU - James, Marianne C.

AU - McMahon, Barry J.

AU - Buckley, Kieran

AU - Piertney, Stuart B.

AU - Höglund, Jacob

N1 - Acknowledgements: We are very thankful to Ahmed Sayadi for helping with the resampling procedures, to Gunilla Engstro¨m for support in the genetic lab, and to Magnus Johansson for helpful discussions. Moreover, we thank the four anonymous reviewers for helpful and constructive advice on this manuscript. Irish feather samples were collected all over Ireland by volunteers from the Irish Grey Partridge Conservation Trust, the National Association of Regional Games Councils of Ireland, the Irish National Park and Wildlife Service, BirdWatch Ireland and red grouse enthusiasts from the Republic of Ireland. We thank staff at the NERC Biomolecular Analysis Facility at Sheffield for SNP genotyping. This study was funded by the Carl Tryggers foundation, the Erasmus Mundus master program in Evolutionary Biology (MEME), the Helge Ax:son Johnson foundation, the Native Species Conservation Committee of Dublin Zoo, Fota Wildlife Park, the UK Natural Environment Research Council and the Swedish Research Council.

PY - 2016/6

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N2 - Studying patterns of intra-specific genetic variation among populations allows for a better understanding of population structure and local adaptation. However, those patterns may differ according to the genetic markers applied, as neutral genetic markers reflect demographic processes and random genetic drift, whereas adaptive markers also carry the footprint of selection. In combination, neutral and adaptive genetic markers permit to assess the relative roles of drift and selection in shaping population structure. Among the best understood adaptive genetic loci are the genes of the major histocompatibility complex (MHC). We here study variation and differentiation at neutral SNP markers and MHC class II genes in red grouse (Lagopus lagopus scotica) from Ireland and Scotland. Irish red grouse populations are fragmented and drastically declining, but red grouse are abundant in Scotland. We find evidence for positive selection acting on the MHC genes and variation in MHC gene copy numbers among Irish individuals. Furthermore, there was significant population differentiation among red grouse from Ireland and Scotland at the neutral SNP markers (FST = 0.084) and the MHC-BLB genes (FST: BLB1 = 0.116, BLB2 = 0.090, BLB3 = 0.104). Differentiation at the MHC-BLB1 was significantly higher than at the neutral SNP markers, suggesting that selection plays an important role in shaping MHC variation, in addition to genetic drift. We speculate that the observed differentiation pattern might be due to local adaptation to different parasite regimes. These findings have strong conservation implications and we advise against the introduction of Scottish red grouse to supplement Irish populations.

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KW - MHC BLB exon 2

KW - Single locus amplification

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Adaptive and neutral genetic differentiation among Scottish and endangered Irish red grouse (Lagopus lagopus scotica)

Abstract

Bibliographical note

Keywords

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