Genomic differentiation across the speciation continuum in three hummingbird species pairs

Abstract

Background: The study of speciation has expanded with the increasing availability and affordability of high-resolution genomic data. How the genome evolves throughout the process of divergence and which regions of the genome are responsible for causing and maintaining that divergence have been central questions in recent work. Here, we use three pairs of species from the recently diverged bee hummingbird clade to investigate differences in the genome at different stages of speciation, using divergence times as a proxy for the speciation continuum.

Results: Population measures of relative differentiation between hybridizing species reveal that different chromosome types diverge at different stages of speciation. Using F_ST as our relative measure of differentiation we found that the sex chromosome shows signs of divergence early in speciation. Next, small autosomes (microchromosomes) accumulate highly diverged genomic regions, while the large autosomes (macrochromosomes) accumulate genomic regions of divergence at a later stage of speciation.

Conclusions: Our finding that genomic windows of elevated F_ST accumulate on small autosomes earlier in speciation than on larger autosomes is counter to the prediction that F_ST increases with size of chromosome (i.e. with decreased recombination rate), and is not represented when weighted average F_ST per chromosome is compared with chromosome size. The results of this study suggest that multiple chromosome characteristics such as recombination rate and gene density combine to influence the genomic locations of signatures of divergence.

Keywords: Divergence; FST; Hummingbird; Polymorphism; Speciation continuum; Speciation genomics; dxy.

Fig. 1

F_ST calculated in 100 kbp windows across the whole genome for three species pairs. Three pairs of hybridizing species have different divergence times (estimated by [51]): top (Selasphorus; 0.97 my), middle (Achilochus; 1.5 my), bottom (Calypte; 2.52 my). Chromosomes alternate in color. Z chromosome (right) has increased F_ST relative to autosomes for all three species pairs. Photograph credits: S. sasin by M. Shattock, CC-BY-SA 2.0; S. rufus by Kaaren Perry, CC-BY 2.0; A. colubris by Dick Ledbetter; A. alexandri by Bill Shreve; C. anna by Becky Matsubara, CC-BY 2.0; C. costae by Daniel Pierce

Fig. 2

Density of windows with different F_ST values separated by chromosome type

Fig. 3

Absolute divergence (d_xy) versus mean nucleotide diversity (π) calculated in 100 kbp windows. d_xy and π were positively correlated in each species pair and chromosome type (a-c). Windows with high F_ST tend to fall in regions with low π relative to d_xy (d-e)

Fig. 4

π versus π between hybridizing species calculated in 100 kbp windows. π was strongly positively correlated with π of its hybridizing species across all chromosome types (a-c). Windows with high F_ST are located where π for both species is low (light blue = high F_ST, dark blue = low F_ST; d-e)

Fig. 5

F_ST for one species pair versus F_ST for another species pair calculated in 100 kbp windows. F_ST is positively correlated across all species pairs and all chromosome types

Fig. 6

F_ST versus chromosome size. Mean F_ST increased with chromosome size only for the most divergent species pair (Calypte). Regression lines, p-values and R² are calculated for all autosomes, excluding the Z chromosome