No abstract

Ecological speciation can proceed despite genetic interchange when selection counteracts the homogenizing effects of migration. We tested predictions of this divergence-with-gene-flow model in Coeligena helianthea and C. bonapartei, 2 parapatric Andean hummingbirds with marked plumage divergence. We sequenced putatively neutral markers (mitochondrial DNA [mtDNA] and nuclear ultraconserved elements [UCEs]) to examine genetic structure and gene flow, and a candidate gene (MC1R) to assess its role underlying divergence in coloration. We also tested the prediction of Gloger’s rule that darker forms occur in more humid environments, and examined morphological variation to assess adaptive mechanisms potentially promoting divergence. Genetic differentiation between species was low in both ND2 and UCEs. Coalescent estimates of migration were consistent with divergence with gene flow, but we cannot reject incomplete lineage sorting reflecting recent speciation as an explanation for patterns of genetic variation. MC1R variation was unrelated to phenotypic differences. Species did not differ in macroclimatic niches but were distinct in morphology. Although we reject adaptation to variation in macroclimatic conditions as a cause of divergence, speciation may have occurred in the face of gene flow driven by other ecological pressures or by sexual selection. Marked phenotypic divergence with no neutral genetic differentiation is remarkable for Neotropical birds, and makes C. helianthea and C. bonapartei an appropriate system in which to search for the genetic basis of species differences employing genomics.

The immunoglobulin-like receptor (KIR) gene family in New World primates (Platyrrhini) has been characterized only in the owl monkey (Aotus sp.). To gain a better understanding of the KIR system in Platyrrhini, we analyzed a KIR haplotype in Ateles geoffroyi, and sequenced KIR complementary DNAs (cDNAs) from other three Atelidae species, Ateles hybridus, Ateles belzebuth, and Lagothrix lagotricha. Atelidae expressed a variable set of activating and inhibitory KIRs that diversified independently from their Catarrhini counterparts. They had a unique mechanism to generate activating receptors from inhibitory ones, involving a single nucleotide deletion in exon 7 and a change in the donor splice site of intron 7. The A. geoffroyi haplotype contained at least six gene models including a pseudogene, two coding inhibitory receptors, and three coding activating receptors. The centromeric region was in a tail-to-tail orientation with respect to the telomeric region. The owl monkey KIR haplotype shared this organization, and in phylogenetic trees, the centromeric genes clustered together with those of A. geoffroyi, whereas their telomeric genes clustered independently. KIR cDNAs from the other Atelidae species conformed to this pattern. Signatures of positive selection were found in residues predicted to interact with the major histocompatibility complex. Such signatures, however, primarily explained variability between paralogous genes but not between alleles in a locus. Atelidae, therefore, has expanded the KIR family in a bimodal fashion, where an inverted centromeric region has remained relatively conserved and the telomeric region has diversified by a rapid process of gene duplication and divergence, likely favored by positive selection for ligand binding.

21Lack of divergence in mitochondrial DNA between species with clear phenotypic differences 22 may be the result of low resolution of markers, incomplete lineage sorting, introgression, or the 23 interplay of various evolutionary mechanisms acting on different traits and genomic regions 24 through time. Previous work revealed that the Andean hummingbirds Coeligena bonapartei and 25 C. helianthea lack genetic divergence in the mitochondrial ND2 gene, which shows variation 26 discordant with coloration phenotype but consistent with geography. We sequenced and analyzed 27 complete mitochondrial genomes for C. b. bonapartei, C. b. consita, C. h. helianthea and C. h. 28 tamai to assess whether patterns revealed by ND2 analyses hold when considering the entire 29 mitogenome, and to shed light into the evolutionary history of these hummingbirds. We found 30 very low genetic differentiation in mitogenomes among the four lineages of Coeligena, 31 confirming patterns based on ND2 data. Estimates of genetic differentiation, phylogenies and 32 haplotype network analyses of complete mitogenomes did not separate phenotypically distinct 33 taxa, but were consistent with a previously described pattern of northern vs. southern divergence 34 along the Cordillera Oriental of Colombia. Mitogenomes of C. b. bonapartei and C. h. helianthea 35 are indistinguishable, suggesting incomplete lineage sorting or strong introgression. 36Mitogenomes of C. b. consita and C. h. tamai are slightly differentiated, but they are more 37 similar to each other than either is to that of its respective nominate subspecies, a result also 38 suggestive of mtDNA introgression despite distinct phenotypic differences. Our results indicate 39 that various evolutionary mechanisms playing out over a complex biogeographic scenario in the 40 Colombian Andes drove divergence in phenotypes and mitochondrial genomes of Coeligena 41 hummingbirds, and lead to alternative hypotheses to be tested with whole-genome analyses. 42 diverge at a faster rate than nuclear DNA -and nuclear-encoded phenotypes -because the 63 effective population size of the former is lower (Ballard and Whitlock, 2004; Moore, 1995). 64However, when selection drives divergence among populations, mtDNA need not diverge sooner 65 than the nuclear genome, resulting in cases where patterns of mitochondrial and nuclear 66 differentiation are not coincident or where phenotypic differentiation exists with little to no 67 mitochondrial differentiation. Furthermore, phenotypically distinct populations may share 68 mtDNA haplotypes because of mitochondrial introgression due to gene flow after divergence 69 (Irwin et al., 2009; Rheindt et al., 2011;Toews and Brelsford, 2012). 70Morphology, plumage, and songs are commonly used to compare populations and inform the 71 species-level taxonomy of birds (Edwards et al., 2005;Remsen, 2005). Morphological plumage patches; Eliason et al., 2020;Parra, 2010), both occurring in the high Andes. One case 95 involves two species of Metallura metaltails (Benham et al., 2...