Biogeographic history of S. corvina
Based on our results and previous work on the genus Sporophila ,
we suggested a possible biogeographic scenario that explains the
distribution, divergence, and patterns of gene flow between subspecies
of S. corvina . The radiation of the genus of Sporophilaseedeaters was initiated around the late Miocene to early Pliocene in
South America, followed by multiple independent bouts of colonization of
Middle America (Mason & Burns, 2013; Mason et al., 2018; Ocampo et al.,
2022a). The ancestral population of the S. corvina likely
diverged from the S. intermedia ancestor, in the late Pliocene,
after a trans-Andes dispersion event (Ocampo et al., 2022a; Stiles,
1996), and dispersed northwards through the Panamanian isthmus (O’Dea et
al., 2016). At this time, the Talamanca mountain range was already
formed to its current elevation (Coates & Obando, 1996), thus imposing
a barrier to lowland bird species. Therefore, the ancestral S.
corvina population likely dispersed through the Pacific and Caribbean
slopes, around the Talamanca mountain range. The population moving north
of Talamanca likely passed through the wetter Caribbean slope reaching
higher latitudes. This all-black lineage may have been isolated (Figure
2B) due to habitat fragmentation associated with forest expansion and
contraction events, as well as wet and arid environmental conditions
associated with climate oscillations during the Pleistocene (e.g.,
Garzón-Orduña et al., 2014). On the other hand, the population south of
the Talamanca mountain range reached a boundary that prevented it from
moving farther north – an ecological and geological boundary known as
the “Tarcoles Line” (Kohlmann & Wilkinson, 2007). This ecotone
separates the tropical wet forest of the Costa Rican South Pacific and
Middle American dry forest, and constrains the distribution of many
species (Kohlmann & Wilkinson, 2007), and is likewise largely
consistent with the current limit of the subspecies range of S. c.
hoffmanni .
Based on this biogeographic scenario, gene flow during secondary contact
between clades, associated with most recent periods of population
expansion, resulted in the currently continuous distribution of S.
c. hoffmanni and S. c. hicksii and the introgression fromS. c. corvina into S. c. hicksii at the Canal in central
Panama. More recently, secondary contact was established in the Central
Valley of Costa Rica, likely favored by deforestation due to human urban
expansion (Biamonte et al., 2011; Joyce, 2006). We found no evidence of
current hybridization between these two subspecies in the Central Valley
region (Figures 3 and 4; Table 3). However, the strength of reproductive
isolation is dynamic, and premating reproductive barriers vary with time
since contact. Reproductive barriers can increase after secondary
contact due to sexual characters displacement (e.g., Jaya et al., 2022),
or the initial reduced gene flow after secondary contact can increase
with time since contact, favoring hybridization and resulting in the
merger of distinct populations (Bettles et al., 2005). Further
behavioral studies in the Central Valley region could provide insights
on the factors maintaining reproductive isolation between subspecies at
the early stages of secondary contact.
CONCLUSIONS
Sporophila corvina from Costa Rica and Panama form three
genetically differentiated groups that are largely consistent with their
current subspecies classifications and geographic distributions. The
three subspecies have established three different contact zones and
hybridize extensively across two of them, regardless of the differences
in plumage patterns of the populations that came into contact (pied vs.
pied or black vs. pied). However, even though plumage divergence does
not act as a strong barrier to gene flow, we found that plumage traits
are divergent and presumably under selection at the contact zones.
Finally, model-based demographic inference suggests that the black
subspecies S. c. corvina diverged in isolation until a recent
secondary contact with S. c. hicksii, resulting in the
hybridization pattern that we see today at one of these contact zones.
Overall, our results suggest that divergence in plumage color is
important in reducing gene flow between these populations, but not
sufficient to stablish complete reproductive isolation. Other factors,
such as reproductive timing or divergence in song, might explain why
hybridization is reduced in one of the contact zones but not in the
others, a pattern of isolation that is likely to change with time.
ACKNOWLEDGMENTS
We thank The University of Alaska Museum, Louisiana State University,
Universidad de Costa Rica, and Smithsonian Tropical Research Institute
collections and their personnel for providing tissue samples used in
this study; SINAC in Costa Rica, and MIAMBIENTE in Panama for granting
research permits; McMillan O., Amador S., Lopez O., STRI’s personnel,
Arce A., Biamonte E., Morrison O., Sánchez C., and Barrantes G. for
assistance and logistical support in Costa Rica and Panama; CIRC (UR)
for access to computing facilities; Searcy W., Campagna, L., the Mason
lab (LSU), and the Uy lab (UR) for valuable comments that improved early
versions of the manuscript; Lastly, we thank our funding sources, the
University of Rochester’s Global Visitor Program (College of Arts and
Sciences), the Hesse student award from the American Ornithological
Society, the Short-term fellowship from the Smithsonian Tropical
Research Institute, and the Kushlan and Savage funds from the University
of Miami (to D. Ocampo), and the Aresty Chair in Tropical Ecology from
the University of Miami (to J.A.C. Uy).
REFERENCES
Abbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J. E.,
Bierne, N., Boughman, J., Brelsford, A., Buerkle, C. A., Buggs, R.,
Butlin, R. K., Dieckmann, U., Eroukhmanoff, F., Grill, A., Cahan, S. H.,
Hermansen, J. S., Hewitt, G., Hudson, A. G., Jiggins, C., …
Zinner, D. (2013). Hybridization and speciation. Journal of
Evolutionary Biology, 26, 229–246.
https://doi.org/10.1111/j.1420-9101.2012.02599.x
Alexander, D. H., Novembre, J., & Lange, K. (2009). Fast model-based
estimation of ancestry in unrelated individuals. Genome Research,
19, 1655–1664. https://doi.org/10.1101/gr.094052.109
Armenta, J. K., Dunn, P. O., & Whittingham, L. A. (2008). Effects of
specimen age on plumage color. The Auk, 125, 803–808.
https://doi.org/10.1525/auk.2008.07006
Baldassarre, D. T., White, T.A., Karubian, J., & Webster, M. S. (2014).
Genomic and morphological analysis of a semipermeable avian hybrid zone
suggests asymmetrical introgression of a sexual signal. Evolution,
68, 2644-2657. https://doi.org/10.1111/evo.12457
Barton, N. H., & Gale, K. S. (1993). Genetic analysis of hybrid zones.
In Harrison, R. G. (Ed.), Hybrid Zones and the Evolutionary
Process (pp. 13–45). Oxford University Press.
Barton, N. H., & Hewitt, G. M. (1985). Analysis of hybrid zones.Annual review of Ecology and Systematics, 16, 113–148.
Bettles, C. M., Docker, M. F., Dufour, B., & Heath, D. D. (2005).
Hybridization dynamics between sympatric species of trout: loss of
reproductive isolation. Journal of Evolutionary Biology, 18,1220–1233. https://doi.org/10.1111/j.1420-9101.2005.00935.x
Biamonte, E., Sandoval, L., Chacón, E., & Barrantes, G. (2011). Effect
of urbanization on the avifauna in a tropical metropolitan area.Landscape Ecology, 26, 183–194.
https://doi.org/10.1007/s10980-010-9564-0
Bocalini, F., Bolívar-Leguizamón, S. D., Silveira, L. F. & Bravo, G. A.
(2021). Comparative phylogeographic and demographic analyses reveal a
congruent pattern of sister relationships between bird populations of
the northern and south-central Atlantic Forest. Molecular
Phylogenetics and Evolution, 154, 106973.
https://doi.org/10.1016/j.ympev.2020.106973
Brumfield, R. T., Jernigan, R. W., McDonald, D. B., & Braun, M. J.
(2001). Evolutionary implications of divergent clines in an avian
(Manacus : aves) hybrid zone. Evolution, 55, 2070–2087.
https://doi.org/10.1111/j.0014-3820.2001.tb01322.x
Buggs, R. (2007). Empirical study of hybrid zone
movement. Heredity, 99, 301–312.
https://doi.org/10.1038/sj.hdy.6800997
Campagna, L., Repenning, M., Silveira, L. F., Fontana, C. S., Tubaro, P.
L., & Lovette. I. J. (2017). Repeated divergent selection on
pigmentation genes in a rapid finch radiation. Science Advances,
3, e1602404. https://doi.org/10.1126/sciadv.1602404
Carantón-Ayala, D., Avendaño, J. E., & Cadena, C. D. (2018).
Hybridization in brushfinches (Atlapetes , Emberizidae) from the
southeast Andes of Colombia: a consequence of habitat disturbance?.Journal of Ornithology, 159, 713–722.
https://doi.org/10.1007/s10336-018-1544-1
Coates, A. G., & Obando, J. A. (1996). The geologic evolution of the
Central American Isthmus. In Jackson, J. B. C., Budd, A. F., & Coates,
A. G. (Eds.). Evolution and Environment in Tropical America (pp.
21–56). University of Chicago Press.
Corbett, E. C., Bravo, G. A., Schunck, F., Naka, L. N., Silveira, L. F.,
& Edwards S. V. (2020). Evidence for the Pleistocene Arc Hypothesis
from genome-wide SNPs in a Neotropical dry forest specialist, the
Rufous-fronted Thornbird (Furnariidae: Phacellodomus rufifrons ).Molecular Ecology, 29, 4457–4472.
https://doi.org/10.1111/mec.15640
Coster, S. S., Welsh, A. B., Costanzo, G., Harding, S. R., Anderson, J.
T., McRae, S. B., & Katzner, T. E. (2018). Genetic analyses reveal
cryptic introgression in secretive marsh bird populations. Ecology
and Evolution, 8, 9870–9879. https://doi.org/10.1002/ece3.4472
Coyne, J. A., & Orr, H. A. (2004). Speciation. Sinauer
Associates.
Crain, B. J., & Fernández, M. (2020). Biogeographical analyses to
facilitate targeted conservation of orchid diversity hotspots in Costa
Rica. Diversity and Distributions, 26, 853–866.
https://doi.org/10.1111/ddi.13062
Crawford, A. J. (2003). Huge populations and old species of Costa Rican
and Panamanian dirt frogs inferred from mitochondrial and nuclear gene
sequences. Molecular Ecology, 12, 2525–2540.
https://doi.org/10.1046/j.1365-294X.2003.01910.x
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E.,
DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S.
T., McVean, G., Durbin, R., & The 1000 Genome Project Analysis Group.
(2011). The variant call format and VCFtools. Bioinformatics, 27,2156–2158. https://doi.org/10.1093/bioinformatics/btr330
Delhey, K., Johnsen, A., Peters, A., Andersson, S., & Kempenaers, B.
(2003). Paternity analysis reveals opposing selection pressures on crown
coloration in the blue tit (Parus caeruleus ). Proceedings
of the Royal Society of London B: Biological Sciences, 270, 2057–2063.
https://doi.org/10.1098/rspb.2003.2460
Derryberry, E. P., Derryberry, G. E., Maley, J. M., & Brumfield, R. T.
(2014). HZAR: hybrid zone analysis using an R software package.Molecular Ecology Resources, 14, 652–663.
https://doi.org/10.1111/1755-0998.12209
Elshire, R. J., Glaubitz, J. C., Sun, Q., Poland, J. A., Kawamoto, K.,
Buckler, E. S., & Mitchell, S. E. (2011). A robust, simple
genotyping-by-sequencing (GBS) approach for high diversity species.PLoS One, 6, e19379. https://doi.org/10.1371/journal.pone.0019379
Endler, J. A. (1977). Geographic variation, speciation, and clines.Monographs in Population Biology, 10, 1–246.
Fitzpatrick, B. M. (2012). Estimating ancestry and heterozygosity of
hybrids using molecular markers. BMC Evolutionary Biology, 12,1–14. https://doi.org/10.1186/1471-2148-12-131
Freeman, B. G., & Montgomery, G. A. (2017). Using song playback
experiments to measure species recognition between geographically
isolated populations: A comparison with acoustic trait analyses.The Auk, 134, 857–870. https://doi.org/10.1642/AUK-17-63.1
Garzón-Orduña, I. J., Benetti-Longhini, J. E., & Brower, A. V. Z.
(2014). Timing the diversification of the Amazonian biota: butterfly
divergences are consistent with Pleistocene refugia. Journal of
Biogeography, 41, 1631–638. https://doi.org/10.1111/jbi.12330
Glaubitz, J. C., Casstevens, T. M., Lu, F., Harriman, J., Elshire, R.
J., Sun, Q., & Buckler, E. S. (2014). TASSEL-GBS: A high capacity
genotyping by sequencing analysis pipeline. PLoS One, 9, e90346.
https://doi.org/10.1371/journal.pone.0090346
Gompert, Z., & Buerkle, C. A. (2009). A powerful regression-based
method for admixture mapping of isolation across the genome of hybrids.Molecular Ecology, 18, 1207–1224.
https://doi.org/10.1111/j.1365-294X.2009.04098.x
Gompert, Z., Mandeville, E. G., & Buerkle, C. A. (2017). Analysis of
population genomic data from hybrid zones. Annual Review of
Ecology, Evolution, and Systematics, 48, 207–229.
https://doi.org/10.1146/annurev-ecolsys-110316-022652
Hackett, S. J. (1996). Molecular phylogenetics and biogeography of
tanagers in the genus Ramphocelus (Aves). Molecular
Phylogenetics and Evolution, 5, 368–382.
https://doi.org/10.1006/mpev.1996.0032
Haffer, J. (1974). Avian speciation in tropical South America.Nuttall Ornithological Club, 14, 1–390.
Harrison, R. G. (1990). Hybrid zones: windows on the evolutionary
process. In Futuyma, D., & Antonovics, J. (Eds.). Oxford Surveys
in Evolutionary Biology (pp. 69–128). Oxford University Press.
Hau, M., Perfito, N., & Moore, I. T. (2008). Timing of breeding in
tropical birds: mechanisms and evolutionary implications.Ornitologia Neotropical, 19 , 39–59.
Hellmayr, C. E. (1938). Catalogue of birds of the Americas. Field
Museum of Natural History Zoology series, 13, 1–662.
Hijmans, R. J. (2019). geosphere: Spherical Trigonometry. R package
version 1.5-10. https://CRAN.R-project.org/package=geosphere.
Irwin, D. E., & Schluter, D. (2021). Hybridization and the coexistence
of species. The American Naturalist, 200, E93-E109.
https://doi.org/10.1086/720365
Jaya, F. R., Tanner, J. C., Whitehead, M. R., Doughty, P., Keogh, J. S.,
Moritz, C. C., & Catullo, R. A. (2022). Population genomics and sexual
signals support reproductive character displacement in Uperoleia(Anura: Myobatrachidae) in a contact zone. Molecular Ecology, 31,4527– 4543. https://doi.org/10.1111/mec.16597
Jiggins, C. D., & Mallet. J. (2000). Bimodal hybrid zones and
speciation. Trends in Ecology and Evolution, 15, 250–255.
https://doi.org/10.1016/S0169-5347(00)01873-5
Jombart, T. (2008). Adegenet: a R package for the multivariate analysis
of genetic markers. Bioinformatics, 24, 1403–1405.
https://doi.org/10.1093/bioinformatics/btn129
Joyce, A. T. (2006). Land use change in Costa Rica: 1996–2006, as
influenced by social, economic, political, and environmental factors.Litografía e imprenta LIL S.A.
Kamm, J., Terhorst, J., Durbin, R., & Song, Y. (2019). Efficiently
inferring the demographic history of many populations with allele count
data. Journal of the American Statistical Association, 115,1472–1487. https://doi.org/10.1080/01621459.2019.1635482
Kohlmann, B., & Wilkinson, M. J. (2007). The Tárcoles Line:
biogeographic effects of the Talamanca Range in lower Central America.Giornale Italiano di Entomologia, 12, 1–30.
Kohlmann, B., Solís, A., Ortwin, E., Soto, X., & Russo, R. (2007).
Biodiversity, conservation, and hotspot atlas of Costa Rica: a dung
beetle perspective (Coleoptera: Scarabaeidae: Scarabaeinae).Zootaxa, 1457, 1–34. https://doi.org/10.11646/zootaxa.1457.1.1
Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with
Bowtie 2. Nature Methods, 9, 357–359.
https://doi.org/10.1038/nmeth.1923
Lipshutz, S. E., Meier, J. I., Derryberry, G. E., Miller, M. J.,
Seehausen, O., & Derryberry, E. P. (2019). Differential introgression
of a female competitive trait in a hybrid zone between sex-role reversed
species. Evolution, 73, 188–201.
https://doi.org/10.1111/evo.13675
Luzuriaga-Aveiga, V. E., Ugarte, M., & Weir, J. T. (2021).
Distinguishing genomic homogenization from parapatric speciation in an
elevationally replacing pair of Ramphocelus tanagers.Molecular Ecology, 30, 5517–5529.
https://doi.org/10.1111/mec.16128
Maia, R. G., Endler, J. A., & White, T. E. (2019). Pavo 2: new tools
for the spectral and spatial analysis of colour in R. Methods in
Ecology and Evolution, 10, 1097–1107.
https://doi.org/10.1111/2041-210X.13174
Marchi, N., Schlichta, F., & Excoffier, L. (2021). Demographic
inference. Current Biology, 31, R276–R279.
https://doi.org/10.1016/j.cub.2021.01.053
Marks, B. D., Hackett, S. J., & Capparella, A. P. (2002). Historical
relationships among Neotropical lowland forest areas of endemism as
determined by mitochondrial DNA sequence variation within the
Wedge-billed Woodcreeper (Aves: Dendrocolaptidae: Glyphorynchus
spirurus ). Molecular Phylogenetics and Evolution, 24, 153–167.
https://doi.org/10.1016/S1055-7903(02)00233-6
Mason, N. A., & Burns K. J. (2013). Molecular phylogenetics of the
neotropical seedeaters and seed-finches (Sporophila, Oryzoborus,
Dolospingus ). Ornitologia Neotropical, 24, 139–155.
Mason, N. A., Olvera-Vital, A., Lovette, I. J., & Navarro-Sigüenza, A.
G. (2018). Hidden endemism, deep polyphyly, and repeated dispersal
across the Isthmus of Tehuantepec: Diversification of the White-collared
Seedeater complex (Thraupidae: Sporophila torqueola ).Ecology and Evolution, 8, 1867–1881.
https://doi.org/10.1002/ece3.3799
Mavárez, J., & Linares, M. (2008). Homoploid hybrid speciation in
animals. Molecular Ecology, 17, 4181–4185.
https://doi.org/10.1111/j.1365-294X.2008.03898.x
Morales-Rozo, A., Tenorio, E. A., Carling, M. D., & Cadena, C. D.
(2017). Origin and cross-century dynamics of an avian hybrid zone.BMC Evolutionary Biology, 17, 257.
https://doi.org/10.1186/s12862-017-1096-7
Moulton, L. L., Vallender, R., Artuso, C., & Koper, N. (2017). The
final frontier: early-stage genetic introgression and hybrid habitat use
in the northwestern extent of the Golden-winged Warbler breeding range.Conservation Genetics, 18, 1481–1487.
https://doi.org/10.1007/s10592-017-0989-8
Nadachowska-Brzyska, K., Li, C., Smeds, L., Zhang, G., & Ellegren, H.
(2015). Temporal dynamics of avian populations during pleistocene
revealed by whole-genome sequences. Current Biology, 25,1375–1380. https://doi.org/10.1016/j.cub.2015.03.047
Nadeau, N. J., Ruiz, M., Salazar, P., Counterman, B., Medina, J. A.,
Ortiz-Zuazaga, H., Morrison, A., McMillan, W. O., Jiggins, C. D., &
Papa, R. (2014). Population genomics of parallel hybrid zones in the
mimetic butterflies, H. melpomene and H. erato .Genome Research, 24, 1316–1333.
https://doi.org/10.1101/gr.169292.113
Ocampo, D., Winker, K., Miller, M. J., Sandoval, L., & Uy, J. A. C.
(2022a). Rapid diversification of the Variable Seedeater superspecies
complex despite widespread gene flow. Molecular Phylogenetics and
Evolution, 173, 107510. https://doi.org/10.1016/j.ympev.2022.107510
[dataset]Ocampo, D., Winker, K., Miller, M. J., Sandoval, L., & Uy,
J. A. C. (2022b). Data from: Replicate hybrid zones suggest a limited
role of plumage in reproductive isolation among subspecies of the
Variable Seedeater (Sporophila corvina ). Dryad.
https://doi.org/10.5061/dryad.fj6q573z5
O’Dea, A., Lessios, H. A., Coates, A. G., Eytan, R. I., Restrepo-Moreno,
S. A., Cione, A. L., Collins, L. S., de Queiroz, A., Farris, D. W.,
Norris, R. D., Stallard, R. F. Woodburne, M. O., Aguilera, O., Aubry,
M., Berggren, W. A., Budd, A. F., Cozzuol, M. A., Coppard, S. E.,
Duque-Caro, H., … & Jackson, J. B. (2016). Formation of the Isthmus
of Panama. Science advances, 2, e1600883.
https://doi.org/10.1126/sciadv.1600883
Olson, S. L. (1981). The nature of variability in the Variable Seedeater
of Panama (Sporophila americana , Emberizinae). Proceedings
of the Biological Society of Washington, 94, 380–390.
Pereira, A. I., & Barrantes, G. (2009). Distribución y densidad de la
avifauna de la Península de Osa, Costa Rica (1990-1991). Revista
de Biologia Tropical, 57, 323–332.
Petkova, D., Novembre, J., & Stephens, M. (2015). Visualizing spatial
population structure with estimated effective migration surfaces.Nature Genetics, 48, 94–103. https://doi.org/10.1038/ng.3464
Price, T. (2008). Speciation in Birds. Roberts and Company.
Robertson, J. M., & Zamudio, K. R. (2009). Genetic diversification,
vicariance, and selection in a polytypic frog. Journal of
Heredity, 100, 715–731. https://doi.org/10.1093/jhered/esp041
Scordato, E. S. C., Smith, C. C. R., Semenov, G. A., Liu, Y., Wilkins,
M. R., Liang, W., Rubtsov, A., Sundev, G., Koyama, K., Turbek, S. P.,
Wunder, M. B., Stricker, C. A., & Safran, R. J. (2020). Migratory
divides coincide with reproductive barriers across replicated avian
hybrid zones above the Tibetan Plateau. Ecology Letters, 23,231–241. https://doi.org/10.1111/ele.13420
Scordato, E. S. C., Wilkins, M. R., Semenov, G., Rubtsov, A. S., Kane,
N. C., & Safran, R. J. (2017). Genomic variation across two Barn
Swallow hybrid zones reveals traits associated with divergence in
sympatry and allopatry. Molecular Ecology, 26, 5676–5691.
https://doi.org/10.1111/mec.14276
Semenov, G. A., Scordato, E. S. C., Khaydarov, D. R., Smith, C. C. R.,
Kane, N. C., & Safran, R. J. (2017). Effects of assortative mate choice
on the genomic and morphological structure of a hybrid zone between two
bird subspecies. Molecular Ecology, 26, 6430–6444.
https://doi.org/10.1111/mec.14376
Skutch, A. F. (1954). Life Histories of Central American Birds.Pacific Coast Avifauna, 31, 448.
Stein, A. C., & Uy, J. A. C. (2006). Unidirectional introgression of a
sexual selected trait across an avian hybrid zone: A role for female
choice?. Evolution, 60, 1476–1485.
https://doi.org/10.1111/j.0014-3820.2006.tb01226.x
Stiles, F. G. (1996). When black plus white equals gray: The nature of
variation in the Variable Seedeater complex (Embarizinae:Sporophila ). Ornitologia Neotropical, 7, 75–107.
Sumner, M. D., Wotherspoon, S. J., & Hindell, M. A. (2009). Bayesian
estimation of animal movement from archival and satellite tags.PLoS one, 4, e7324. https://doi.org/10.1371/journal.pone.0007324
Szymura, J. M., & Barton, N. H. (1986). Genetic analysis of a hybrid
zone between the fire-bellied toads, Bombina bombina and B.
variegata , near Cracow in southern Poland. Evolution, 40,1141–1159. https://doi.org/10.1111/j.1558-5646.1986.tb05740.x
Todesco, M., Pascual, M. A., Owens, G. L., Ostevik, K. L., Moyers, B.
T., Hübner, S., Heredia, S. M., Hahn, M. A., Caseys, C., Bock, D. G., &
Rieseberg, L. H. (2016). Hybridization and extinction.Evolutionary Applications, 9, 892–908.
https://doi.org/10.1111/eva.12367
Uy, J. A. C., & Stein, A. C. (2007). Variable visual habitats may
influence the spread of colourful plumage across an avian hybrid zone.Journal of Evolutionary Biology, 20, 1847–1858.
https://doi.org/10.1111/j.1420-9101.2007.01378.x
Venegas-Anaya, M., Crawford, A. J., Galván, A. H. E., Sanjur, O. I.,
Densmore, L. D., & Bermingham, E. (2008). Mitochondrial DNA
phylogeography of Caiman crocodilus in Mesoamerica and South
America. Journal of Experimental Zoology, 309, 614–627.
https://doi.org/10.1002/jez.502
Walsh, J., Shriver, W. G., Olsen, B. J., & Kovach, A. I. (2016).
Differential introgression and the maintenance of species boundaries in
an advanced generation avian hybrid zone. BMC Evolutionary
Biology, 16, 65. https://doi.org/10.1186/s12862-016-0635-y
While, G. M., Michaelides, S., Heathcote, R. J., MacGregor, H. E.,
Zajac, N., Beninde, J., Carazo, P., Pérez I de Lanuza, G., Sacchi, R.,
Zuffi, M. A., Horváthová, T., Fresnillo, B., Schulte, U., Veith, M.,
Hochkirch, A., & Uller. T. (2015). Sexual selection drives asymmetric
introgression in wall lizards. Ecology Letters, 18, 1366–1375.
https://doi.org/10.1111/ele.12531
Zamudio, K. R., & Greene, H. W. (1997). Phylogeography of the
bushmaster (Lachesis muta : Viperidae): implications for
neotropical biogeography, systematics, and conservation.Biological Journal of the Linnean Society, 62, 421–442.
https://doi.org/10.1111/j.1095-8312.1997.tb01634.x
DATA AVAILABILITY STATEMENT
SNPs and phenotypic data are available on Dryad data repository (Ocampo
et al., 2022b). “Scorvina_SNPs_1.vcf” and “Scorvina_SNPs_2.vcf”
contain the SNPs data sets according to our two filtering criteria.
“Scorvina_B2.txt” including plumage brightness per patch per
individual. “Scorvina_morph.txt” including morphometric data. Related
metadata can be found in Table S1 (including georeferences in decimal
degrees and date/month/year of sampling event).
BENEFIT-SHARING STATEMENT
Benefits Generated: A collaborative research was developed with
scientists and institutions providing genetic samples, all collaborators
are included as co-authors. Other contributors to the research are
included in the ACKNOWLEDGEMENTS section. The results of the research
have been shared with the scientific community.
AUTHOR CONTRIBUTIONS
D. Ocampo and A. Uy conceptualized the study; D. Ocampo, K. Winker, M.
Miller, and L. Sandoval collected the samples; D. Ocampo collected
phenotypic data and performed data analyses. D. Ocampo and A. Uy drafted
the manuscript with significant input of all authors. All authors have
read and approved the final manuscript.