Impact of Landscape on Host–Parasite Genetic Diversity and Distribution Using the Puumala orthohantavirus–Bank Vole System
Abstract
:1. Introduction
2. Materials and Methods
2.1. Samples Preparation
2.2. Microsatellite Genotyping of Voles
2.3. Landscape Characteristics of the Study Sites
2.4. Screening for PUUV
2.5. RT-PCR and Sequencing of the PUUV Genome
2.6. Molecular Signatures of Selection of PUUV Strains
2.7. Phylogenetic Analysis of PUUV Strains
2.8. Local Genetic Diversity
2.9. Large-Scale Genetic Structure
2.10. Landscape Analyses
3. Results
3.1. Detection and Genetic Diversity of PUUV and Bank Voles from the French Ardennes
3.2. Phylogenetic Analysis of PUUV Strains from the French Ardennes
3.3. Spatial Genetic Structure of PUUV and Bank Voles from the French Ardennes
3.4. Effect of Landscape Features and Bank Vole Population Dynamics on PUUV Prevalence and Diversity
4. Discussion
4.1. Genetic Diversity of PUUV and Bank Voles from the French Ardennes
4.2. Phylogenetic Analysis of PUUV Strains from the French Ardennes
4.3. Spatial Genetic Structure of PUUV and Bank Voles from the French Ardennes
4.4. Effect of Landscape Features and Bank Vole Population Dynamics on PUUV Prevalence and Diversity
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Sites | Longitude | Latitude | Proportion of Forested Habitat (%) | Forest Contiguity Index | Shape Index | Edge Density (m/km2) | No. of Patches | Distance to Next Patch (m) |
---|---|---|---|---|---|---|---|---|
Hargnies | 4.7950 | 49.9961 | 0.838 | 0.93 | 37.3 | 883.7 | 14 | 200 |
Woiries | 4.7664 | 49.9037 | 0.861 | 0.93 | 37.3 | 936.4 | 9 | 200 |
Renwez | 4.6113 | 49.8590 | 0.632 | 0.93 | 37.3 | 14484 | 10 | 200 |
Cliron | 4.6204 | 49.8032 | 0.022 | 0.85 | 19.4 | 169.7 | 2 | 956 |
Elan | 4.7674 | 49.6536 | 0.585 | 0.71 | 4.1 | 1203.3 | 3 | 200 |
Cassine | 4.7945 | 49.5752 | 0.421 | 0.84 | 3.5 | 1226.3 | 3 | 208 |
Sauville | 4.8003 | 49.5454 | 0.252 | 0.82 | 3.0 | 901.9 | 4 | 411 |
Croix-aux-Bois | 4.8385 | 49.4166 | 0.596 | 0.82 | 2.8 | 900.2 | 9 | 355 |
Boult-aux-Bois | 4.9215 | 49.4136 | 0.187 | 0.76 | 2.5 | 1311.8 | 8 | 445 |
Briquenay | 4.9109 | 49.3937 | 0.169 | 0.78 | 2.7 | 904.5 | 7 | 493 |
Genome Segment | No. of Strains | S (43–1341 nt) | M (2180–2632 nt) | L (577–987 nt) | |
---|---|---|---|---|---|
Analyzed length | Nucleotides (nt) | 33 | 1299 | 453 | 411 |
Amino acids (aa) | 33 | 433 | 151 | 137 | |
No. of substitutions | Nt polymorphic sites (total no. of mutations) | 33 | 178 (185) | 62 (63) | 69 (71) |
Nt singleton variable sites | 33 | 29 | 10 | 2 | |
Nt parsimony informative sites | 33 | 149 | 52 | 67 | |
Aa variable sites | 33 | 11 | 4 | 5 | |
Genetic diversity (%) | Nucleotides (nt) | 33 | 14.2 | 13.9 | 17.3 |
Amino acids (aa) | 33 | 2.5 | 2.7 | 2.7 | |
No. of nt substitutions (%) | Hargnies | 10 | 29 (2.2) | 11 (2.4) | 13 (3.2) |
Woiries | 3 | 60 (4.6) | 25 (5.5) | 28 (6.8) | |
Renwez | 5 | 10 (0.8) | 0 | 0 | |
Cliron | 2 | 0 | 0 | 0 | |
Elan | 2 | 4 (0.3) | 1 (0.2) | 1 (0.2) | |
Cassine | 6 | 10 (0.8) | 2 (0.4) | 0 | |
Croix-aux-Bois | 3 | 8 (0.6) | 4 (0.9) | 3 (0.7) | |
Boult-aux-Bois | 2 | 4 (0.3) | 1 (0.2) | 0 | |
No. of aa substitutions (%) | Hargnies | 10 | 3 (0.7) | 0 | 0 |
Woiries | 3 | 1 (0.2) | 0 | 2 (1.5) | |
Renwez | 5 | 2 (0.5) | 0 | 0 | |
Cliron | 2 | 0 | 0 | 0 | |
Elan | 2 | 0 | 0 | 0 | |
Cassine | 6 | 1 (0.2) | 0 | 0 | |
Croix-aux-Bois | 3 | 0 | 1 (0.7) | 1 (0.7) | |
Boult-aux-Bois | 2 | 0 | 0 | 0 |
Segment | Strains Group | n | π | h | Hd | Tajima’s D | Fu and Li’s D | Fu and Li’s F |
---|---|---|---|---|---|---|---|---|
Ardennes | 33 | 0.036 | 30 | 0.994 | 0.10 | 0.64 | 0.50 | |
S | CE | 99 | 0.098 | 89 | 0.997 | 0.53 | 0.62 | 0.70 |
All PUUV | 189 | 0.138 | 178 | 0.999 | 0.46 | −0.04 | 0.25 | |
Ardennes | 33 | 0.043 | 14 | 0.922 | 0.99 | 0.59 | 0.86 | |
M | CE | 63 | 0.096 | 29 | 0.960 | 0.75 | 1.12 | 1.17 |
All PUUV | 117 | 0.147 | 76 | 0.987 | 0.62 | 0.88 | 0.91 | |
Ardennes | 33 | 0.051 | 12 | 0.898 | 0.75 | 1.70 *(p < 0.02) | 1.63 *( p < 0.05) | |
L | CE | 52 | 0.106 | 26 | 0.953 | 0.49 | 0.68 | 0.73 |
All PUUV | 88 | 0.160 | 61 | 0.984 | 0.31 | 0.67 | 0.62 |
Source | df | SS | MS | Est. var. | % | Stat. | p (Rand ≥ Data) | |
---|---|---|---|---|---|---|---|---|
PUUV | Among forest massifs | 2 | 896.9 | 448 | 41.3 | 65 | PhiRT = 0.647 | 0.001 |
Among localities | 5 | 313.1 | 62.6 | 14.8 | 23 | PhiPR = 0.661 | 0.001 | |
Within localities | 25 | 190.9 | 7.6 | 7.6 | 12 | PhiPR = 0.661 | 0.001 | |
Total | 32 | 1400 | 63.8 | 100 | PhiPT = 0.880 | 0.001 | ||
Bank voles | Among forest massifs | 2 | 49.8 | 24.9 | 0.04 | 1 | FRT = 0.006 | 0.001 |
Among localities | 7 | 111.9 | 16 | 0.1 | 2 | FSR = 0.020 | 0.001 | |
Within localities | 300 | 2199.2 | 7.3 | 0.3 | 4 | FSR = 0.020 | 0.001 | |
Total | 619 | 4435.8 | 7.2 | 100 | FST = 0.026 | 0.001 |
Source | Landscape | Vole | |||
---|---|---|---|---|---|
% Forest | Contiguity | Shape | Genetic Diversity | ||
Voles | Genetic diversity | + ** | NS | NS | |
PUUV prevalence | + ** | + ** | NS | + *** | |
PUUV | Nucleotide diversity (NtDiv) | + ** | + * | NS | NS |
Amino-acid diversity (AaDiv) | NS | NS | NS | NS |
Genome Segment | PUUV Lineages | No. of Strains | No. of nt Substitutions (Variable Sites) | Genetic Diversity (%) | aa Substitutions (%) |
---|---|---|---|---|---|
S (43–1341 nt; 1299 nt, 433 aa) | All known PUUV | 189 | 913 (584) | 70.3 | 73 (16.9) |
Danish (DAN) | 3 | 87 (85) | 6.7 | 17 (3.9) | |
Latvian (LAT) | 5 | 178 (174) | 13.7 | 1 (0.2) | |
North-Scandinavian (N-SCA) | 23 | 335 (294) | 25.8 | 20 (4.6) | |
South-Scandinavian (S-SCA) | 8 | 261 (251) | 20.1 | 17 (3.9) | |
Russian (RUS) | 16 | 364 (319) | 28.0 | 29 (6.7) | |
Finnish (FIN) | 27 | 429 (361) | 33.0 | 52 (12.0) | |
Alpe-Adrian (ALAD) | 8 | 138 (133) | 10.6 | 13 (3.0) | |
Central European (CE) | 99 | 567 (435) | 43.6 | 31 (7.2) | |
M (2180–2632 nt; 453 nt, 151 aa) | All knwon PUUV | 117 | 258 (167) | 57.0 | 13 (8.6) |
Danish (DAN) | 3 | 21 (21) | 4.6 | 3 (2.0) | |
Latvian (LAT) | 1 | - | - | - | |
North-Scandinavian (N-SCA) | 8 | 128 (113) | 31.8 | 9 (6.0) | |
South-Scandinavian (S-SCA) | 4 | 81 (77) | 17.9 | 3 (2.0) | |
Russian (RUS) | 11 | 145 (121) | 32.0 | 8 (5.3) | |
Finnish (FIN) | 15 | 144 (124) | 31.8 | 8 (5.3) | |
Alpe-Adrian (ALAD) | 12 | 80 (71) | 17.7 | 6 (4.0) | |
Central European (CE) | 63 | 146 (127) | 32.2 | 12 (7.9) | |
L (577–987 nt; 411 nt, 137 aa) | All known PUUV | 88 | 304 (202) | 74.0 | 21 (15.3) |
Danish (DAN) | 3 | 32 (32) | 7.8 | 4 (2.9) | |
Latvian (LAT) | 4 | 91 (83) | 22.1 | 8 (5.8) | |
North-Scandinavian (N-SCA) | 2 | 61 (61) | 14.8 | 10 (7.3) | |
South-Scandinavian (S-SCA) | 0 | - | - | - | |
Russian (RUS) | 7 | 122 (108) | 29.7 | 12 (8.8) | |
Finnish (FIN) | 17 | 105 (95) | 25.5 | 8 (5.8) | |
Alpe-Adrian (ALAD) | 3 | 21 (21) | 7.8 | 0 | |
Central European (CE) | 52 | 173 (140) | 42.1 | 15 (10.9) | |
North-Scandinavian (N-SCA) | 23 | 335 (294) | 25.8 | 20 (4.6) | |
South-Scandinavian (S-SCA) | 8 | 261 (251) | 20.1 | 17 (3.9) | |
Alpe-Adrian (ALAD) | 8 | 138 (133) | 10.6 | 13 (3.0) | |
Central European (CE) | 99 | 567 (435) | 43.6 | 31 (7.2) |
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Razzauti, M.; Castel, G.; Cosson, J.-F. Impact of Landscape on Host–Parasite Genetic Diversity and Distribution Using the Puumala orthohantavirus–Bank Vole System. Microorganisms 2021, 9, 1516. https://doi.org/10.3390/microorganisms9071516
Razzauti M, Castel G, Cosson J-F. Impact of Landscape on Host–Parasite Genetic Diversity and Distribution Using the Puumala orthohantavirus–Bank Vole System. Microorganisms. 2021; 9(7):1516. https://doi.org/10.3390/microorganisms9071516
Chicago/Turabian StyleRazzauti, Maria, Guillaume Castel, and Jean-François Cosson. 2021. "Impact of Landscape on Host–Parasite Genetic Diversity and Distribution Using the Puumala orthohantavirus–Bank Vole System" Microorganisms 9, no. 7: 1516. https://doi.org/10.3390/microorganisms9071516