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Effect of the Central American Isthmus on gene flow and divergence of the American crocodile (Crocodylus acutus)Avila-Cervantes, JoseArias, CarlosVenegas-Anaya, MiryamVargas, MartaLarsson, Hans C. E.McMillan, W. OwenDOI: info:10.1111/evo.14139v. 75No. 2245–259
Avila-Cervantes, Jose, Arias, Carlos, Venegas-Anaya, Miryam, Vargas, Marta, Larsson, Hans C. E., and McMillan, W. Owen. 2021. "Effect of the Central American Isthmus on gene flow and divergence of the American crocodile (Crocodylus acutus)." Evolution 75 (2):245– 259. https://doi.org/10.1111/evo.14139
ID: 157996
Type: article
Authors: Avila-Cervantes, Jose; Arias, Carlos; Venegas-Anaya, Miryam; Vargas, Marta; Larsson, Hans C. E.; McMillan, W. Owen
Abstract: The final formation of the Central American Isthmus (CAI) about 3.5 million years ago altered global ocean circulation, connected North and South America terrestrial biotas, and established the Caribbean Sea. The nature of this event creates a natural scenario to test vicariance, divergence, and speciation by allopatry. Studies have shown the effect of the CAI on marine and terrestrial species, but none have examined a large-bodied amphibious taxon. We used RAD sequencing on populations of the American crocodile (Crocodylus acutus) to study the genomic variation of C. acutus on both sides of the CAI, infer its demographic history, and measure the effect of the opening of the Panama Canal. Our results showed three genomic clusters: (1) Caribbean and the Panama Canal, (2) Pacific coast, and (3) Coiba island. The estimated divergence times between the Caribbean and Pacific populations are about 20,000 years ago, which is younger than the formation of the CAI, coinciding with the Last Glacial Maximum. We hypothesize the glacial/interglacial cycles facilitated gene flow between the Caribbean and Pacific crocodile populations after the formation of the CAI, masking any genomic divergence the CAI may have caused. There is no evidence of gene flow associated with the opening of the Panama Canal.
The Microbiome of Neotropical Water Striders and Its Potential Role in CodiversificationCastillo, Anakena M.Saltonstall, KristinArias, Carlos F.Chavarria, Karina A.Ramírez-Camejo, Luis A.Mejía, Luis C.De León, Luis F.DOI: info:10.3390/insects11090578v. 11No. 9578
Castillo, Anakena M., Saltonstall, Kristin, Arias, Carlos F., Chavarria, Karina A., Ramírez-Camejo, Luis A., Mejía, Luis C., and De León, Luis F. 2020. "The Microbiome of Neotropical Water Striders and Its Potential Role in Codiversification." Insects 11 (9):578. https://doi.org/10.3390/insects11090578
ID: 156941
Type: article
Authors: Castillo, Anakena M.; Saltonstall, Kristin; Arias, Carlos F.; Chavarria, Karina A.; Ramírez-Camejo, Luis A.; Mejía, Luis C.; De León, Luis F.
Abstract: Insects host a highly diverse microbiome, which plays a crucial role in insect life. However, the composition and diversity of microbiomes associated with Neotropical freshwater insects is virtually unknown. In addition, the extent to which diversification of this microbiome is associated with host phylogenetic divergence remains to be determined. Here, we present the first comprehensive analysis of bacterial communities associated with six closely related species of Neotropical water striders in Panama. We used comparative phylogenetic analyses to assess associations between dominant bacterial linages and phylogenetic divergence among species of water striders. We found a total of 806 16S rRNA amplicon sequence variants (ASVs), with dominant bacterial taxa belonging to the phyla Proteobacteria (76.87%) and Tenericutes (19.51%). Members of the α- (e.g., Wolbachia) and γ- (e.g., Acinetobacter, Serratia) Proteobacteria, and Mollicutes (e.g., Spiroplasma) were predominantly shared across species, suggesting the presence of a core microbiome in water striders. However, some bacterial lineages (e.g., Fructobacillus, Fluviicola and Chryseobacterium) were uniquely associated with different water strider species, likely representing a distinctive feature of each species' microbiome. These findings indicate that both host identity and environmental context are important drivers of microbiome diversity in water striders. In addition, they suggest that diversification of the microbiome is associated with diversification in water striders. Although more research is needed to establish the evolutionary consequences of host-microbiome interaction in water striders, our findings support recent work highlighting the role of bacterial community host-microbiome codiversification.
Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing PatternsConcha, CarolinaWallbank, Richard W. R.Hanly, Joseph J.Fenner, JenniferLivraghi, LucaRivera, Edgardo SantiagoPaulo, Daniel F.Arias, CarlosVargas, MartaSanjeev, ManuMorrison, ColinTian, DavidAguirre, PaolaFerrara, SabrinaFoley, JessicaPardo-Diaz, CarolinaSalazar, CamiloLinares, MauricioMassardo, DarliCounterman, Brian A.Scott, Maxwell J.Jiggins, Chris D.Papa, RiccardoMartin, ArnaudMcMillan, W. O.DOI: info:10.1016/j.cub.2019.10.0101–19
Concha, Carolina, Wallbank, Richard W. R., Hanly, Joseph J., Fenner, Jennifer, Livraghi, Luca, Rivera, Edgardo Santiago, Paulo, Daniel F., Arias, Carlos, Vargas, Marta, Sanjeev, Manu, Morrison, Colin, Tian, David, Aguirre, Paola, Ferrara, Sabrina, Foley, Jessica, Pardo-Diaz, Carolina, Salazar, Camilo, Linares, Mauricio, Massardo, Darli, Counterman, Brian A., Scott, Maxwell J., Jiggins, Chris D., Papa, Riccardo, Martin, Arnaud, and McMillan, W. O. 2019. "Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns." Current Biology 1– 19. https://doi.org/10.1016/j.cub.2019.10.010
ID: 153256
Type: article
Authors: Concha, Carolina; Wallbank, Richard W. R.; Hanly, Joseph J.; Fenner, Jennifer; Livraghi, Luca; Rivera, Edgardo Santiago; Paulo, Daniel F.; Arias, Carlos; Vargas, Marta; Sanjeev, Manu; Morrison, Colin; Tian, David; Aguirre, Paola; Ferrara, Sabrina; Foley, Jessica; Pardo-Diaz, Carolina; Salazar, Camilo; Linares, Mauricio; Massardo, Darli; Counterman, Brian A.; Scott, Maxwell J.; Jiggins, Chris D.; Papa, Riccardo; Martin, Arnaud; McMillan, W. O.
Abstract: To what extent can we predict how evolution occurs? Do genetic architectures and developmental processes canalize the evolution of similar outcomes in a predictable manner? Or do historical contingencies impose alternative pathways to answer the same challenge? Examples of Müllerian mimicry between distantly related butterfly species provide natural replicates of evolution, allowing us to test whether identical wing patterns followed parallel or novel trajectories. Here, we explore the role that the signaling ligand WntA plays in generating mimetic wing patterns in Heliconius butterflies, a group with extraordinary mimicry-related wing pattern diversity. The radiation is relatively young, and numerous cases of wing pattern mimicry have evolved within the last 2.5–4.5 Ma. WntA is an important target of natural selection and is one of four major effect loci that underlie much of the pattern variation in the group. We used CRISPR/Cas9 targeted mutagenesis to generate WntA-deficient wings in 12 species and a further 10 intraspecific variants, including three co-mimetic pairs. In all tested butterflies, WntA knockouts affect pattern broadly and cause a shift among every possible scale cell type. Interestingly, the co-mimics lacking WntA were very different, suggesting that the gene networks that pattern a wing have diverged considerably among different lineages. Thus, although natural selection channeled phenotypic convergence, divergent developmental contexts between the two major Heliconius lineages opened different developmental routes to evolve resemblance. Consequently, even under very deterministic evolutionary scenarios, our results underscore a surprising unpredictability in the developmental paths underlying convergence in a recent radiation.
Inheritance, distribution and genetic differentiation of a color polymorphism in Panamanian populations of the tortoise beetle, Chelymorpha alternans (Coleoptera: Chrysomelidae)Strickland, Lynette R.Arias, Carlos F.Rodriguez, ViterboJohnston, J. S.McMillan, W. O.Windsor, Donald M.DOI: info:10.1038/s41437-018-0149-zv. 122558–569
Strickland, Lynette R., Arias, Carlos F., Rodriguez, Viterbo, Johnston, J. S., McMillan, W. O., and Windsor, Donald M. 2019. "Inheritance, distribution and genetic differentiation of a color polymorphism in Panamanian populations of the tortoise beetle, Chelymorpha alternans (Coleoptera: Chrysomelidae)." Heredity 122:558– 569. https://doi.org/10.1038/s41437-018-0149-z
ID: 148942
Type: article
Authors: Strickland, Lynette R.; Arias, Carlos F.; Rodriguez, Viterbo; Johnston, J. S.; McMillan, W. O.; Windsor, Donald M.
Abstract: Intraspecific variation maintained in natural populations has long intrigued scientists and naturalists. One form of this variation, color polymorphisms, provide a rich opportunity to connect genotypic and phenotypic diversity within an ecological and evolutionary context. The existence of color polymorphisms in Panamanian populations of the Neotropical tortoise beetle, Chelymorpha alternans, has been suspected but never systematically explored. To characterize geographic distribution and underlying genetics we sampled a total of 3819 beetles from 28 sites across Panama, quantifying five distinct phenotypes. Two phenotypes, the "metallic" and "rufipennis" are the most widely distributed phenotypes, occurring in nearly all collecting sites. The "veraguensis" phenotype was found to be restricted to the Western end of the Isthmus and the "militaris" phenotypes restricted to sites east of the canal. Controlled matings between phenotypes and reared offspring revealed no indications of reproductive barriers, even among phenotypes which do not co-occur in nature. Color pattern phenotype is largely controlled by Mendelian assortment of four alleles competing at a single locus. A clear dominance hierarchy exists among alleles, with two being co-dominant. Genomic scans from 32 individuals revealed low levels of genetic differentiation, with a small fraction of the genome showing a high degree of divergence. The easily observed variation among populations, simple genetic architecture, and rearing capabilities, make this a promising system for investigating proximate and ultimate factors of phenotypic variation.
Gene flow and Andean uplift shape the diversification of Gasteracantha cancriformis (Araneae: Araneidae) in Northern South AmericaSalgado-Roa, FabianPardo-Diaz, CarolinaLasso, EloisaArias, Carlos F.Solferini, Vera NisakaSalazar, CamiloDOI: info:10.1002/ece3.4237v. 8No. 147131–7142
Salgado-Roa, Fabian, Pardo-Diaz, Carolina, Lasso, Eloisa, Arias, Carlos F., Solferini, Vera Nisaka, and Salazar, Camilo. 2018. "Gene flow and Andean uplift shape the diversification of Gasteracantha cancriformis (Araneae: Araneidae) in Northern South America." Ecology and Evolution 8 (14):7131– 7142. https://doi.org/10.1002/ece3.4237
ID: 148691
Type: article
Authors: Salgado-Roa, Fabian; Pardo-Diaz, Carolina; Lasso, Eloisa; Arias, Carlos F.; Solferini, Vera Nisaka; Salazar, Camilo
Abstract: The Andean uplift has played a major role in shaping the current Neotropical biodiversity. However, in arthropods other than butterflies, little is known about how this geographic barrier has impacted species historical diversification. Here, we examined the phylogeography of the widespread color polymorphic spider Gasteracantha cancriformis to evaluate the effect of the northern Andean uplift on its divergence and assess whether its diversification occurred in the presence of gene flow. We inferred phylogenetic relationships and divergence times in G. cancriformis using mitochondrial and nuclear data from 105 individuals in northern South America. Genetic diversity, divergence, and population structure were quantified. We also compared multiple demographic scenarios for this species using a model-based approach (phrapl) to determine divergence with or without gene flow. At last, we evaluated the association between genetic variation and color polymorphism. Both nuclear and mitochondrial data supported two well-differentiated clades, which correspond to populations occurring on opposite sides of the Eastern cordillera of the Colombian Andes. The final uplift of this cordillera was identified as the most likely force that shaped the diversification of G. cancriformis in northern South America, resulting in a cis- and trans-Andean phylogeographic structure for the species. We also found shared genetic variation between the cis- and trans-Andean clades, which is better explained by a scenario of historical divergence in the face of gene flow. This has been likely facilitated by the presence of low-elevation passes across the Eastern Colombian cordillera. Our work constitutes the first example in which the Andean uplift coupled with gene flow influenced the evolutionary history of an arachnid lineage.
A new subspecies in a Heliconius butterfly adaptive radiation (Lepidoptera: Nymphalidae)Arias, Carlos F.Giraldo, NathaliaMcMillan, W. OwenJiggins, Chris D.Salazar, CamiloDOI: info:10.1093/zoolinnean/zlw010v. 180No. 4805–818
Arias, Carlos F., Giraldo, Nathalia, McMillan, W. Owen, Jiggins, Chris D., and Salazar, Camilo. 2017. "A new subspecies in a Heliconius butterfly adaptive radiation (Lepidoptera: Nymphalidae)." Zoological Journal of the Linnean Society 180 (4):805– 818. https://doi.org/10.1093/zoolinnean/zlw010
ID: 141341
Type: article
Authors: Arias, Carlos F.; Giraldo, Nathalia; McMillan, W. Owen; Jiggins, Chris D.; Salazar, Camilo
Evolution of novel mimicry rings facilitated by adaptive introgression in tropical butterfliesEnciso-Romero, JuanPardo-Díaz, CarolinaMartin, Simon H.Arias, Carlos F.Linares, MauricioMcMillan, William OwenJiggins, Chris D.Salazar, CamiloDOI: info:10.1111/mec.14277v. 26No. 195160–5172
Enciso-Romero, Juan, Pardo-Díaz, Carolina, Martin, Simon H., Arias, Carlos F., Linares, Mauricio, McMillan, William Owen, Jiggins, Chris D., and Salazar, Camilo. 2017. "Evolution of novel mimicry rings facilitated by adaptive introgression in tropical butterflies." Molecular ecology 26 (19):5160– 5172. https://doi.org/10.1111/mec.14277
ID: 143778
Type: article
Authors: Enciso-Romero, Juan; Pardo-Díaz, Carolina; Martin, Simon H.; Arias, Carlos F.; Linares, Mauricio; McMillan, William Owen; Jiggins, Chris D.; Salazar, Camilo
Complex modular architecture around a simple toolkit of wing pattern genesVan Belleghem, Steven M.Rastas, PasiPapanicolaou, AlexieMartin, Simon H.Arias, Carlos F.Supple, Megan A.Hanly, Joseph J.Mallet, JamesLewis, James J.Hines, Heather M.Ruiz, MayteSalazar, CamiloLinares, MauricioMoreira, Gilson R. P.Jiggins, Chris D.Counterman, Brian A.McMillan, W. O.Papa, RiccardoDOI: info:10.1038/s41559-016-0052v. 1No. 352
Van Belleghem, Steven M., Rastas, Pasi, Papanicolaou, Alexie, Martin, Simon H., Arias, Carlos F., Supple, Megan A., Hanly, Joseph J., Mallet, James, Lewis, James J., Hines, Heather M., Ruiz, Mayte, Salazar, Camilo, Linares, Mauricio, Moreira, Gilson R. P., Jiggins, Chris D., Counterman, Brian A., McMillan, W. O., and Papa, Riccardo. 2017. "Complex modular architecture around a simple toolkit of wing pattern genes." Nature Ecology & Evolution 1 (3):52. https://doi.org/10.1038/s41559-016-0052
ID: 143557
Type: article
Authors: Van Belleghem, Steven M.; Rastas, Pasi; Papanicolaou, Alexie; Martin, Simon H.; Arias, Carlos F.; Supple, Megan A.; Hanly, Joseph J.; Mallet, James; Lewis, James J.; Hines, Heather M.; Ruiz, Mayte; Salazar, Camilo; Linares, Mauricio; Moreira, Gilson R. P.; Jiggins, Chris D.; Counterman, Brian A.; McMillan, W. O.; Papa, Riccardo
Abstract: Identifying the genomic changes that control morphological variation and understanding how they generate diversity is a major goal of evolutionary biology. In Heliconius butterflies, a small number of genes control the development of diverse wing colour patterns. Here, we used full-genome sequencing of individuals across the Heliconius erato radiation and closely related species to characterize genomic variation associated with wing pattern diversity. We show that variation around colour pattern genes is highly modular, with narrow genomic intervals associated with specific differences in colour and pattern. This modular architecture explains the diversity of colour patterns and provides a flexible mechanism for rapid morphological diversification.
Genomics at the evolving species boundaryArias, Carlos F.Van Belleghem, StevenMcMillan, W. OwenDOI: info:10.1016/j.cois.2015.10.004v. 137–15
Arias, Carlos F., Van Belleghem, Steven, and McMillan, W. Owen. 2016. "Genomics at the evolving species boundary." Current Opinion in Insect Science 13:7– 15. https://doi.org/10.1016/j.cois.2015.10.004
ID: 137754
Type: article
Authors: Arias, Carlos F.; Van Belleghem, Steven; McMillan, W. Owen
Abstract: Molecular studies on hybridization date back to Dobzhansky who compared chromosomal banding patterns to determine if interspecific gene flow occurred in nature 1]. Now, the advent of high-throughput sequencing provides increasingly fine insights into genomic differentiation between incipient taxa that are changing our view of adaptation and speciation and the links between the two. Empirical data from hybridizing taxa demonstrate highly heterogeneous patterns of genomic differentiation. Although underlining reasons for this heterogeneity are complex, studies of hybridizing taxa offers some of the best insights into the regions of the genome under divergent selection and the role these regions play in species boundaries. The challenge moving forward is to develop a better theoretical framework that fully leverages these powerful natural experiments.
Phylogeography of Heliconius cydno and its closest relatives: disentangling their origin and diversificationArias, Carlos F.Salazar, CamiloRosales, ClaudiaKronforst, Marcus R.Linares, MauricioBermingham, EldredgeMcMillan, William OwenDOI: info:10.1111/mec.12844v. 23No. 164137–4152
Arias, Carlos F., Salazar, Camilo, Rosales, Claudia, Kronforst, Marcus R., Linares, Mauricio, Bermingham, Eldredge, and McMillan, William Owen. 2014. "Phylogeography of Heliconius cydno and its closest relatives: disentangling their origin and diversification." Molecular ecology 23 (16):4137– 4152. https://doi.org/10.1111/mec.12844
ID: 127109
Type: article
Authors: Arias, Carlos F.; Salazar, Camilo; Rosales, Claudia; Kronforst, Marcus R.; Linares, Mauricio; Bermingham, Eldredge; McMillan, William Owen
Sharp genetic discontinuity across a unimodal Heliconius hybrid zoneArias, Carlos F.Rosales, ClaudiaSalazar, CamiloCastaño, JullyBermingham, EldredgeLinares, MauricioMcMillan, William OwenDOI: info:10.1111/j.1365-294X.2012.05746.xv. 21No. 235778–5794
Arias, Carlos F., Rosales, Claudia, Salazar, Camilo, Castaño, Jully, Bermingham, Eldredge, Linares, Mauricio, and McMillan, William Owen. 2012. "Sharp genetic discontinuity across a unimodal Heliconius hybrid zone." Molecular ecology 21 (23):5778– 5794. https://doi.org/10.1111/j.1365-294X.2012.05746.x
ID: 112832
Type: article
Authors: Arias, Carlos F.; Rosales, Claudia; Salazar, Camilo; Castaño, Jully; Bermingham, Eldredge; Linares, Mauricio; McMillan, William Owen
Abstract: Hybrid zones are powerful natural systems to study evolutionary processes to gain an understanding of adaptation and speciation. In the Cauca Valley (Colombia), two butterfly races, Heliconius cydno cydnides and Heliconius cydno weymeri, meet and hybridize. We characterized this hybrid zone using a combination of mitochondrial DNA (mtDNA) sequences, amplified fragment length polymorphisms (AFLPs), microsatellites and sequences for nuclear loci within and outside of the genomic regions that cause differences in wing colour pattern. The hybrid zone is largely composed of individuals of mixed ancestry. However, there is strong genetic discontinuity between the hybridizing races in mtDNA and, to a lesser extent, in all nuclear markers surveyed. The mtDNA clustering of H. c. cydnides with the H. cydno race from the Magdalena Valley and H. c. weymeri with the H. cydno race from the pacific coast suggests that H. c. cydnides colonized the Cauca Valley from the north, whereas H. c. weymeri did so by crossing the Andes in the southern part, implying a secondary contact origin. Colonization of the valley by H. cydno was accompanied by mimicry shift. Strong ecological isolation, driven by locally adaptive differences in mimetic wing patterns, is playing an important role in maintaining the hybrid zone. However, selection on wing pattern alone is not sufficient to explain the genetic discontinuity observed. There is evidence for differences in male mating preference, but the contribution of additional barriers needs further investigation. Overall, our results support the idea that speciation is a cumulative process, where the combination of multiple isolation barriers, combined with major phenotypic differences, facilitates population divergence in face of gene flow.
A hybrid zone provides evidence for incipient ecological speciation in Heliconius butterfliesArias, Carlos F.Muñoz, Astrid G.Jiggins, Chris D.Mavárez, JesúsBermingham, EldredgeLinares, MauricioDOI: info:10.1111/j.1365-294X.2008.03934.xv. 17No. 214699–4712
Arias, Carlos F., Muñoz, Astrid G., Jiggins, Chris D., Mavárez, Jesús, Bermingham, Eldredge, and Linares, Mauricio. 2008. "A hybrid zone provides evidence for incipient ecological speciation in Heliconius butterflies." Molecular ecology 17 (21):4699– 4712. https://doi.org/10.1111/j.1365-294X.2008.03934.x
ID: 75849
Type: article
Authors: Arias, Carlos F.; Muñoz, Astrid G.; Jiggins, Chris D.; Mavárez, Jesús; Bermingham, Eldredge; Linares, Mauricio