Shallow genetic divergence and distinct phenotypic differences between two Andean hummingbirds: Speciation with gene flow?

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.

Speciation rates are positively correlated with the rate of plumage color evolution in hummingbirds

“…Even though we found an association between speciation and color evolution rates, we cannot affirm causality in ei-ther direction. Answering this fascinating question will require population-level (Winger and Bates 2015) and genomic studies (Palacios et al 2019), but coming to a consensus across species may prove unlikely, because evolutionary pressures vary strongly among lineages. It is likely that additional evolutionary forces such as niche differentiation and the evolution of other traits help explain speciation rates (Temeles 2000;Ritchie 2007;Parra 2010;Maia et al 2016;Folk et al 2019).…”

“…However, this seems inverted in polytypic species with visually different subspecies and even populations that belong to the same lineage in current taxonomy (e.g., Coeligena torquata and Metallura tyrianthina). Furthermore, vast color differences may not even match molecular divergence in differentiated species recognized by current taxonomy (e.g., Palacios et al 2019). Additionally, we evaluated the rate at which color properties change, not the color properties themselves, which reduces the impact of color-based taxonomy by providing a measure of the evolution of a species' trait, encompassing the entire lineage's evolutionary history.…”

“…Furthermore, vast color differences may not even match molecular divergence in differentiated species recognized by current taxonomy (e.g., Palacios et al. 2019). Additionally, we evaluated the rate at which color properties change, not the color properties themselves, which reduces the impact of color‐based taxonomy by providing a measure of the evolution of a species’ trait, encompassing the entire lineage's evolutionary history.…”

Phylogenetic analysis of the Neotropical Albitarsis Complex based on mitogenome data

“…janconnae clade began between 0.64 and 1.35 mya. This period was also highly important in shaping interspecific diversification in other mosquito complexes (Nuneztovari Complex) [ 87 ] and forest birds [ 88 ] and intraspecific clade diversification in forest species of amphibians [ 89 ], birds [ 90 ], and mammals [ 91 ] in northern South America. One of the species that emerged, An.…”

The genomic revolution and species delimitation in birds (and other organisms): gene flow matters, but what about other evolutionary forces?

“…Of course, we do not deny the enormous power of genomics to aid species delimitation in birds, allowing the elucidation of species boundaries not observable with few genetic markers. For example, phenotypically distinct hummingbirds from the northern Andes in the genus Coeligena are not distinguishable with mitochondrial genomes nor with variable regions flanking nuclear ultraconserved elements (Palacios et al 2019;Palacios et al in review), yet complete genomes clearly separate taxa in line with traditional plumage-based taxonomy (Palacios et al unpubl. data).…”