Historical demography of Trichothraupis melanops (Aves: Thraupidae) and the Pleistocene Atlantic Forest biogeography

Andrea Agustina Turner; Natalia Trujillo-Arias; Gustavo Sebastián Cabanne

doi:10.56178/eh.v38i2.1431

Artículos Publicado 01 diciembre 2023 https://doi.org/10.56178/eh.v38i2.1431

Demografía histórica de Trichothraupis melanops (Aves: Thraupidae) y biogeografía de la Selva Atlántica en el Pleistoceno

Demografía histórica Filogeografía Pleistoceno Selva Atlántica Trichothraupis

Andrea Agustina Turner Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”– MACN-CONICET, Av. Ángel Gallardo 470, Buenos Aires C1405DJR, Argentina

Natalia Trujillo-Arias Instituto de investigación en recursos biológicos Alexander von Humboldt, (111311, Colombia, Cundinamarca, Bogotá, Av. Circunvalar #16-20)

Gustavo Sebastián Cabanne Instituto de investigación en recursos biológicos Alexander von Humboldt, (111311, Colombia, Cundinamarca, Bogotá, Av. Circunvalar #16-20)

Resumen

Los ciclos climáticos del Pleistoceno afectaron la distribución de la vegetación de diferentes biomas, condicionando la distribución y evolución de la fauna asociada. Muchos estudios sobre organismos de la Selva Atlántica (SA) sugieren que los ciclos glaciales e interglaciales del Pleistoceno han producido poblaciones demográficamente estables en la región central de la selva y poblaciones inestables en sus regiones del sur (conocido como modelo Carnaval-Moritz). Estudiamos la estructura filogeográfica de un paseriforme que se distribuye en la SA, el Frutero de Anteojos Negros (Trichothraupis melanops, Thraupidae), y evaluamos preguntas relacionadas con la historia de la SA. Analizamos tres genes independientes, dos nucleares y uno mitocondrial, utilizando métodos de genética de poblaciones basados en estadísticas sumarias y métodos filogeográficos tradicionales. Nuestros resultados sugieren que T. melanops comparte características filogeográficas con otros taxones de la SA. Si bien se encontró un gradiente de tamaño poblacional efectivo entre las poblaciones del centro y del sur, lo que concuerda con los resultados de otros estudios filogeográficos y el modelo de refugios (el modelo Carnaval-Moritz), no hay evidencia de un gradiente de diversidad genética. Además, hemos encontrado que las poblaciones de T. melanops presentan la dinámica demográfica esperada por el modelo Carnaval-Moritz: la población del centro-sur resultó ser la que presenta mayores signos de expansión demográfica reciente, en comparación con las poblaciones central y de la costa sur. Aunque esta especie es ecológicamente generalista y poco sensible a la fragmentación y degradación forestal, ha sido impactada por el dinamismo histórico de la Selva Atlántica.

PDF (Inglés)

Referencias

dos Anjos L (2006) Bird Species Sensitivity in a Fragmented Landscape of the Atlantic Forest in Southern Brazil. Biotropica 38(2): 229–234. https://doi.org/10.1111/j.1744-7429.2006.00122.x
Bandelt H, Forster P and Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16(1):37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Batalha-Filho H, Cabanne GS and Miyaki CY (2012) Phylogeography of an Atlantic forest passerine reveals demographic stability through the last glacial maximum. Molecular Phylogenetics and Evolution 65:892–902. https://doi.org/10.1016/j.ympev.2012.08.010
Batalha-Filho H, Fjeldså J, Fabre P-H and Miyaki CY (2013) Connections between the Atlantic and the Amazonian Forest avifaunas represent distinct historical events. Journal of Ornithology 154:41–50. https://doi.org/10.1007/s10336-012-0866-7
Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A, Heled J, Jones G, Kühnert D, De Maio N, Matschiner M, Mendes FK, Müller NF, Ogilvie HA, du Plessis L, Popinga A, Rambaut A, Rasmussen D, Siveroni I, Suchard MA, Wu C-H, Xie D, Zhang C, Stadler T and Drummond AJ (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS computational biology 15(4), e1006650. https://doi.org/10.1371/journal.pcbi.1006650
Bukowski B, Campagna L, Rodríguez-Cajarville MJ, Cabanne GS, Tubaro PL AND Lijtmaer DA (2023) The role of glaciations in the evolutionary history of a widely distributed Neotropical open habitat bird. Journal of Biogeography 30:71-86. https://doi.org/10.1111/jbi.14738
Burns KJ and Racicot RA (2009) Molecular Phylogenetics of a Clade of Lowland Tanagers: Implications for Avian Participation in the Great American Interchange. The Auk 126(3):635-648. https://doi.org/10.1525/auk.2009.08195
Cabanne GS, Campagna L, Trujillo-Arias N, Naoki K, Gómez I, Miyaki CY, Santos FR, Dantas GPM, Aleixo A, Claramunt S, Rocha A, Caparroz R, Lovette IJ and Tubaro PL (2019) Phylogeographic variation within the Buff-browed Foliage-gleaner (Aves: Furnariidae: Syndactyla rufosuperciliata) supports an Andean-Atlantic forests connection via the Cerrado. Molecular phylogenetics and evolution 133:198-213. https://doi.org/10.1016/j.ympev.2019.01.011
Cabanne GS, d’Horta FM, Sari EHR, Santos FR and Miyaki CY (2008) Nuclear and mitochondrial phylogeography of the Atlantic forest endemic Xiphorhynchus fuscus (Aves: Dendrocolaptidae): Biogeography and systematics implications. Molecular Phylogenetics and Evolution, 49:760–773. https://doi.org/10.1016/j.ympev.2008.09.013
Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT and Moritz C (2009) Stability predicts genetic diversity in the Brasilian Atlantic forest hotspot. Science 323(5915):785–789. https://doi.org/10.1126/science.1166955
Carnaval AC and Moritz C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brasilian Atlantic forest. Journal of Biogeography 35:1187-1201. https://doi.org/10.1111/j.1365-2699.2007.01870.x
Costa L (2003) The historical bridge between between the Amazon and the Atlantic forest of Brasil: a study of molecular phylogeography with small mammals. Journal of Biogeography 30:71-86. https://doi.org/10.1046/j.1365-2699.2003.00792.x
Costa LP and Leite YLR (2013) Historical fragmentation shaping vertebrate diversification in the Atlantic forest biodiversity hotspot. Pp. 283-306 in: Patterson BD and Costa LP (eds) Bones, Clones and Biomes: The History and Geography of Recent Neotropical Mammals. Chicago University Press, Chicago
Cracraft J and Prum RO (1988) Patterns and processes of diversifications: speciation and historical congruence in some Neotropical birds. Evolution, 42:603–620. https://doi.org/10.1111/j.1558-5646.1988.tb04164.x
Excoffier L and Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147(2):915-25. https://doi.org/10.1093/genetics/147.2.915
Galindo Leal C and Câmara I de G (2003) The Atlantic forest of South America: biodiversity status, threats, and outlook. State of the Hotspots. Island Press, Washington
Guillot G, Mortier F and Estoup A (2005) Geneland: A program for landscape genetics. Molecular Ecology Notes 5:712-715. https://doi.org/10.1111/j.1471-8286.2005.01031.x
Haffer J (1969) Speciation in Amazonian Forest birds. Science 165(3889):131-137. https://doi.org/10.1126/science.165.3889.13
Haffer J and Prance GT (2001) Climatic forcing of evolution in Amazonia during the Cenozoic: on the refuge theory of biotic differentiation. Amazoniana 16:579–607
IUCN (2021) The IUCN Red List of Threatened Species. Version 2021-1. (URL: https://www.iucnredlist.org)
Lima-Rezende CA, Cabanne GS, Rocha AV, Carboni M, Zink RM and Caparroz R (2022) A comparative phylogenomic analysis of birds reveals heterogeneous differentiation processes among Neotropical savannas. Molecular Ecology 31(12):3451–3467. https://doi.org/10.1111/mec.16487
Moritz C, Patton JL, Schneider CJ and Smith TB (2000) Diversification of Rainforest Faunas: An Integrated Molecular Approach. Annual Review of Ecology and Systematics 31(1):533–563. https://doi.org/10.1146/annurev.ecolsys.31.1.533
Oksanen J, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E and Wagner H (2020) Vegan: Community Ecology Package. R package version 2.5-7 (URL: https://CRAN.R-project.org/package=vegan)
Papadopoulou A, Anastasiou I and Vogler AP (2010) Revisiting the insect mitochondrial molecular clock: the mid-Aegean trench calibration. Molecular Biology and Evolution 27:1659–1672. https://doi.org/10.1093/molbev/msq051
Ramos-Onsins S and Rozas J (2002) Statistical Properties of New Neutrality Tests Against Population Growth. Molecular Biology and Evolution 19(12):2092-2100. https://doi.org/10.1093/oxfordjournals.molbev.a004034
Raposo do Amaral F, Thom G, Lima-Ribeiro MS, Alvarado-Serrano DF, Montesanti JAC, Pellegrino KCM, Miyaki CY, Hickerson MJ and Maldonado-Coelho M (2021) Rugged relief and climate promote isolation and divergence between two neotropical cold-associated birds. Evolution, 75:2371-2387. https://doi.org/10.1111/evo.14318
Ribon R, Simon JE and De Mattos GT (2003) Bird extinctions in Atlantic forest fragments of the Vicosa region, southeastern Brazil. Conservation Biology 17(6):1827–1839. https://doi.org/10.1111/j.1523-1739.2003.00377.x
Ridgely R and Tudor G (2009) Field guide to the songbirds of South America: the passerines. Mildred Wyatt-World series in ornithology (1st edition). Austin: University of Texas Press. Trichothraupis melanops, p. 621, lámina 104(4)
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE and Sánchez-Gracia A (2017) DnaSP v6: DNA Sequence Polymorphism Analysis of Large Datasets. Molecular Biology and Evolution 34:3299-3302. https://doi.org/10.1093/molbev/msx248
RStudio Team (2015) RStudio: Integrated Develoment for R. RStudio, Inc., Boston, MA
Rull V and Carnval AC (2020) Neotropical Diversification: Patterns and Processes. Springer, Switzerland
Sudhir K, Glen S and Koichiro T (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33(7):1870-1874. https://doi.org/10.1093/molbev/msw054
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–95. https://doi.org/10.1093/genetics/123.3.585
Thom G, Gehara M, Smith BT, Miyaki CY and Raposo do Amaral F (2021) Microevolutionary dynamics show tropical valleys are deeper for montane birds of the Atlantic Forest. Nature Communication 12, 6269. https://doi.org/10.1038/s41467-021-26537-9
Trujillo-Arias N, Calderón L, Santos FR, Miyaki CY, Aleixo A, Witt CC, Tubaro PL, and Cabanne GS (2018) Forest corridors between the central Andes and the southern Atlantic forest enabled dispersal and peripatric diversification without niche divergence in a passerine. Molecular Phylogenetics and Evolution 128:221–232. https://doi.org/10.1016/j.ympev.2018.08.005
Trujillo-Arias N, Rodríguez-Cajarville MJ, Sari E, Miyaki CY, Santos FR, Witt CC, Barreira AS, Gómez I, Naoki K, Tubaro PL and Cabanne GS (2020) Evolution between forest macrorefugia is linked to discordance between genetic and morphological variation in Neotropical passerines. Molecular Phylogenetics and Evolution 149, 106849. https://doi.org/10.1016/j.ympev.2020.106849
Watterson GA (1978) The homozygosity test of neutrality. Genetics 88:405-417. https://doi.org/10.1093/genetics/88.2.405
Yednock BK and Neigel JE (2014) Detecting Selection in the Blue Crab, Callinectes sapidus, Using DNA Sequence Data from Multiple Nuclear Protein-Coding Genes. PLoS ONE 9(6):e99081. https://doi.org/10.1371/journal.pone.0099081
Zeng K, Fu Y-X, Shi S and Wu C-I (2006) Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174:1431–1439. https://doi.org/10.1534/genetics.106.061432
Zeng K, Mano S, Shi S AND Wu C-I (2007a) Comparisons of site- and haplotype-frequency methods for detecting positive selection. Molecular Biology and Evolution 24:1562–1574. https://doi.org/10.1093/molbev/msm078
Zeng K, Shi S and Wu CI (2007b) Compound tests for the detection of hitchhiking under positive selection. Molecular Biology and Evolution 24(8):1898-1908. https://doi.org/10.1093/molbev/msm119

Cómo citar

Andrea Agustina Turner, Natalia Trujillo-Arias, Gustavo Sebastián Cabanne (2023). Demografía histórica de Trichothraupis melanops (Aves: Thraupidae) y biogeografía de la Selva Atlántica en el Pleistoceno. El Hornero, Vol. 38 Núm. 2 (2023), 7-17. https://doi.org/10.56178/eh.v38i2.1431

Descargas

965Visualizaciones del texto completo

1Formatos

Licencia: CC BY-NC 4.0

[1] dos Anjos L (2006) Bird Species Sensitivity in a Fragmented Landscape of the Atlantic Forest in Southern Brazil. Biotropica 38(2): 229–234. https://doi.org/10.1111/j.1744-7429.2006.00122.x

[2] Bandelt H, Forster P and Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16(1):37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

[3] Batalha-Filho H, Cabanne GS and Miyaki CY (2012) Phylogeography of an Atlantic forest passerine reveals demographic stability through the last glacial maximum. Molecular Phylogenetics and Evolution 65:892–902. https://doi.org/10.1016/j.ympev.2012.08.010

[4] Batalha-Filho H, Fjeldså J, Fabre P-H and Miyaki CY (2013) Connections between the Atlantic and the Amazonian Forest avifaunas represent distinct historical events. Journal of Ornithology 154:41–50. https://doi.org/10.1007/s10336-012-0866-7

[5] Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A, Heled J, Jones G, Kühnert D, De Maio N, Matschiner M, Mendes FK, Müller NF, Ogilvie HA, du Plessis L, Popinga A, Rambaut A, Rasmussen D, Siveroni I, Suchard MA, Wu C-H, Xie D, Zhang C, Stadler T and Drummond AJ (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS computational biology 15(4), e1006650. https://doi.org/10.1371/journal.pcbi.1006650

[6] Bukowski B, Campagna L, Rodríguez-Cajarville MJ, Cabanne GS, Tubaro PL AND Lijtmaer DA (2023) The role of glaciations in the evolutionary history of a widely distributed Neotropical open habitat bird. Journal of Biogeography 30:71-86. https://doi.org/10.1111/jbi.14738

[7] Burns KJ and Racicot RA (2009) Molecular Phylogenetics of a Clade of Lowland Tanagers: Implications for Avian Participation in the Great American Interchange. The Auk 126(3):635-648. https://doi.org/10.1525/auk.2009.08195

[8] Cabanne GS, Campagna L, Trujillo-Arias N, Naoki K, Gómez I, Miyaki CY, Santos FR, Dantas GPM, Aleixo A, Claramunt S, Rocha A, Caparroz R, Lovette IJ and Tubaro PL (2019) Phylogeographic variation within the Buff-browed Foliage-gleaner (Aves: Furnariidae: Syndactyla rufosuperciliata) supports an Andean-Atlantic forests connection via the Cerrado. Molecular phylogenetics and evolution 133:198-213. https://doi.org/10.1016/j.ympev.2019.01.011

[9] Cabanne GS, d’Horta FM, Sari EHR, Santos FR and Miyaki CY (2008) Nuclear and mitochondrial phylogeography of the Atlantic forest endemic Xiphorhynchus fuscus (Aves: Dendrocolaptidae): Biogeography and systematics implications. Molecular Phylogenetics and Evolution, 49:760–773. https://doi.org/10.1016/j.ympev.2008.09.013

[10] Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT and Moritz C (2009) Stability predicts genetic diversity in the Brasilian Atlantic forest hotspot. Science 323(5915):785–789. https://doi.org/10.1126/science.1166955

[11] Carnaval AC and Moritz C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brasilian Atlantic forest. Journal of Biogeography 35:1187-1201. https://doi.org/10.1111/j.1365-2699.2007.01870.x

[12] Costa L (2003) The historical bridge between between the Amazon and the Atlantic forest of Brasil: a study of molecular phylogeography with small mammals. Journal of Biogeography 30:71-86. https://doi.org/10.1046/j.1365-2699.2003.00792.x

[13] Costa LP and Leite YLR (2013) Historical fragmentation shaping vertebrate diversification in the Atlantic forest biodiversity hotspot. Pp. 283-306 in: Patterson BD and Costa LP (eds) Bones, Clones and Biomes: The History and Geography of Recent Neotropical Mammals. Chicago University Press, Chicago

[14] Cracraft J and Prum RO (1988) Patterns and processes of diversifications: speciation and historical congruence in some Neotropical birds. Evolution, 42:603–620. https://doi.org/10.1111/j.1558-5646.1988.tb04164.x

[15] Excoffier L and Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

[16] Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147(2):915-25. https://doi.org/10.1093/genetics/147.2.915

[17] Galindo Leal C and Câmara I de G (2003) The Atlantic forest of South America: biodiversity status, threats, and outlook. State of the Hotspots. Island Press, Washington

[18] Guillot G, Mortier F and Estoup A (2005) Geneland: A program for landscape genetics. Molecular Ecology Notes 5:712-715. https://doi.org/10.1111/j.1471-8286.2005.01031.x

[19] Haffer J (1969) Speciation in Amazonian Forest birds. Science 165(3889):131-137. https://doi.org/10.1126/science.165.3889.13

[20] Haffer J and Prance GT (2001) Climatic forcing of evolution in Amazonia during the Cenozoic: on the refuge theory of biotic differentiation. Amazoniana 16:579–607

[21] IUCN (2021) The IUCN Red List of Threatened Species. Version 2021-1. (URL: https://www.iucnredlist.org)

[22] Lima-Rezende CA, Cabanne GS, Rocha AV, Carboni M, Zink RM and Caparroz R (2022) A comparative phylogenomic analysis of birds reveals heterogeneous differentiation processes among Neotropical savannas. Molecular Ecology 31(12):3451–3467. https://doi.org/10.1111/mec.16487

[23] Moritz C, Patton JL, Schneider CJ and Smith TB (2000) Diversification of Rainforest Faunas: An Integrated Molecular Approach. Annual Review of Ecology and Systematics 31(1):533–563. https://doi.org/10.1146/annurev.ecolsys.31.1.533

[24] Oksanen J, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E and Wagner H (2020) Vegan: Community Ecology Package. R package version 2.5-7 (URL: https://CRAN.R-project.org/package=vegan)

[25] Papadopoulou A, Anastasiou I and Vogler AP (2010) Revisiting the insect mitochondrial molecular clock: the mid-Aegean trench calibration. Molecular Biology and Evolution 27:1659–1672. https://doi.org/10.1093/molbev/msq051

[26] Ramos-Onsins S and Rozas J (2002) Statistical Properties of New Neutrality Tests Against Population Growth. Molecular Biology and Evolution 19(12):2092-2100. https://doi.org/10.1093/oxfordjournals.molbev.a004034

[27] Raposo do Amaral F, Thom G, Lima-Ribeiro MS, Alvarado-Serrano DF, Montesanti JAC, Pellegrino KCM, Miyaki CY, Hickerson MJ and Maldonado-Coelho M (2021) Rugged relief and climate promote isolation and divergence between two neotropical cold-associated birds. Evolution, 75:2371-2387. https://doi.org/10.1111/evo.14318

[28] Ribon R, Simon JE and De Mattos GT (2003) Bird extinctions in Atlantic forest fragments of the Vicosa region, southeastern Brazil. Conservation Biology 17(6):1827–1839. https://doi.org/10.1111/j.1523-1739.2003.00377.x

[29] Ridgely R and Tudor G (2009) Field guide to the songbirds of South America: the passerines. Mildred Wyatt-World series in ornithology (1st edition). Austin: University of Texas Press. Trichothraupis melanops, p. 621, lámina 104(4)

[30] Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE and Sánchez-Gracia A (2017) DnaSP v6: DNA Sequence Polymorphism Analysis of Large Datasets. Molecular Biology and Evolution 34:3299-3302. https://doi.org/10.1093/molbev/msx248

[31] RStudio Team (2015) RStudio: Integrated Develoment for R. RStudio, Inc., Boston, MA

[32] Rull V and Carnval AC (2020) Neotropical Diversification: Patterns and Processes. Springer, Switzerland

[33] Sudhir K, Glen S and Koichiro T (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33(7):1870-1874. https://doi.org/10.1093/molbev/msw054

[34] Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–95. https://doi.org/10.1093/genetics/123.3.585

[35] Thom G, Gehara M, Smith BT, Miyaki CY and Raposo do Amaral F (2021) Microevolutionary dynamics show tropical valleys are deeper for montane birds of the Atlantic Forest. Nature Communication 12, 6269. https://doi.org/10.1038/s41467-021-26537-9

[36] Trujillo-Arias N, Calderón L, Santos FR, Miyaki CY, Aleixo A, Witt CC, Tubaro PL, and Cabanne GS (2018) Forest corridors between the central Andes and the southern Atlantic forest enabled dispersal and peripatric diversification without niche divergence in a passerine. Molecular Phylogenetics and Evolution 128:221–232. https://doi.org/10.1016/j.ympev.2018.08.005

[37] Trujillo-Arias N, Rodríguez-Cajarville MJ, Sari E, Miyaki CY, Santos FR, Witt CC, Barreira AS, Gómez I, Naoki K, Tubaro PL and Cabanne GS (2020) Evolution between forest macrorefugia is linked to discordance between genetic and morphological variation in Neotropical passerines. Molecular Phylogenetics and Evolution 149, 106849. https://doi.org/10.1016/j.ympev.2020.106849

[38] Watterson GA (1978) The homozygosity test of neutrality. Genetics 88:405-417. https://doi.org/10.1093/genetics/88.2.405

[39] Yednock BK and Neigel JE (2014) Detecting Selection in the Blue Crab, Callinectes sapidus, Using DNA Sequence Data from Multiple Nuclear Protein-Coding Genes. PLoS ONE 9(6):e99081. https://doi.org/10.1371/journal.pone.0099081

[40] Zeng K, Fu Y-X, Shi S and Wu C-I (2006) Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174:1431–1439. https://doi.org/10.1534/genetics.106.061432

[41] Zeng K, Mano S, Shi S AND Wu C-I (2007a) Comparisons of site- and haplotype-frequency methods for detecting positive selection. Molecular Biology and Evolution 24:1562–1574. https://doi.org/10.1093/molbev/msm078

[42] Zeng K, Shi S and Wu CI (2007b) Compound tests for the detection of hitchhiking under positive selection. Molecular Biology and Evolution 24(8):1898-1908. https://doi.org/10.1093/molbev/msm119