Selection on a plumage‐associated gene block maintains a stable boundary between two warbler species

A new paper pub­lished in Evol­u­tion Let­ters exam­ines the gen­om­ic under­pin­nings of spe­ci­ation by study­ing the diver­gent pig­ment traits of two warbler spe­cies in a hybrid zone. Here, lead author Dr Silu Wang tells us more.

What kind of gen­om­ic regions are most import­ant for spe­ci­ation of song­birds? The genes under­ly­ing spe­cies-spe­cif­ic plumage col­or­a­tion are increas­ingly high­lighted in recent whole gen­ome sequen­cing research. How­ever, the evol­u­tion­ary forces that render col­or gene vari­ation at spe­cies bound­ar­ies remain elu­sive. In our new paper pub­lished in Evol­u­tion Let­ters, we found selec­tion-dis­pers­al bal­ance shap­ing the evol­u­tion of a small (2Mb) col­or gene block (ASIP-RALY) at the spe­cies bound­ary of two wood warbler spe­cies, Seto­phaga occi­dental­is (Fig­ure 1 A) and S. town­sendi (Fig­ure 1 B). This ASIP-RALY col­or gene block is asso­ci­ated with vari­ation in a suite of plumage col­or­a­tion traits among hybrids in the hybrid zone of the two spe­cies in the Pacific North­w­est (Fig­ure 1 C & D). 

Fig­ure 1. Pho­tos from the field: (A) Seto­phaga occi­dental­is and (B) S. town­sendi, two wood warbler spe­cies; (C & D) Douglas fir forests in the Cas­cade Moun­tain range, where the work was car­ried out; (E & F) hybrids of the two wood warbler spe­cies with inter­me­di­ate plumage col­or patterns.

Deep in the Douglas fir forests around the Cas­cade moun­tain range (Fig­ure 1 C & D), Chris Wood and Siev­ert Rohwer (Uni­ver­sity of Wash­ing­ton) sampled warblers among sites in this hybrid zone 20 years ago. They found many hybrids (Fig­ure 1 E & F) with inter­me­di­ate plumage col­or pat­terns to the par­ent­al spe­cies (Fig­ure 1 A & B), except that most of the hybrids have sim­il­ar cheek col­or­a­tion as S. occi­dental­is (Fig­ure 1 A). Wood and Rohwer inferred that there should be a single locus, with the S. occi­dental­is allele being dom­in­ant, reg­u­lat­ing the cheek col­or vari­ation between species. 

In 2015–16 sum­mer, we sampled the hybrid warblers in the same sites again to under­stand the evol­u­tion of these hybrid pop­u­la­tions. By gen­o­typ­ing birds at tens of thou­sands of DNA vari­ants and examin­ing the asso­ci­ation with plumage vari­ation in the hybrid zone, we con­firmed Wood and Rohwer­’s infer­ence that a gene block pre­dom­in­antly explains the cheek col­or vari­ation among birds in the hybrid zone, with the S. occi­dental­is allele being dom­in­ant. This gene block con­tains three genes: ASIP, EIF2S2, and RALY (ASIP-RALY gene block). In addi­tion, we found that this gene block explains vari­ation in oth­er traits as well: crown col­or­a­tion, flank strik­ing, and the intens­ity of the yel­low breast. 

To invest­ig­ate wheth­er selec­tion is main­tain­ing the dif­fer­ences between spe­cies in this genet­ic region, we used a cline meth­od that we estab­lished before. Across the hybrid zone, the dis­tri­bu­tion of spe­cies-spe­cif­ic char­ac­ters (gen­om­ic or phen­o­typ­ic) are expec­ted to form a cline, which widens over time only if dis­pers­al is shap­ing the con­tact zone (Fig­ure 2, left). How­ever, selec­tion against hybrids would coun­ter­act the widen­ing effect of dis­pers­al (Fig­ure 2, right), keep­ing the cline nar­row­er than expec­ted by a neut­ral dif­fu­sion pro­cess. By track­ing the hybrid zone over two dec­ades and at least 12 gen­er­a­tions of the warbler pop­u­la­tions, we found inter­est­ing cline dynamics. 

Fig­ure 2. Con­cep­tu­al illus­tra­tion of spe­cies-spe­cif­ic char­ac­ter dis­tri­bu­tions shaped either by neut­ral dif­fu­sion or selection.

Although gen­om­ic cline con­forms with the neut­ral dif­fu­sion expect­a­tion, the plumage cline and the ASIP-RALY cline are con­sist­ent with the altern­at­ive selec­tion mod­el. Moreover, the change of ASIP-RALY cline was even smal­ler than the plumage cline, in which the cline of the recent sampling peri­od was almost nar­row­er than the his­tor­ic­al cline. Such res­ult sug­gests that selec­tion act­ing dir­ectly at ASIP-RALY gene block coun­ter­acts dis­pers­al, keep­ing the plumage cline and the hybrid zone nar­row over time. Hence, this par­tic­u­lar small genet­ic region explains much of the dif­fer­en­ti­ation and phen­o­typ­ic dif­fer­en­ti­ation between these species. 

Dr Silu Wang is a postdoc­tor­al research­ers at the Uni­ver­sity of Cali­for­nia, Berke­ley. The ori­gin­al art­icle is freely avail­able to read and down­load here.