What happens when populations having different pairs of sex chromosomes hybridize?

Post by Xuel­ing Yi

A recent study pub­lished in Evol­u­tion Let­ters explores hybrid­iz­a­tion in the nine-spined stickle­back, a fish whose pop­u­la­tions have dif­fer­ent sex chro­mo­somes. Author Xuel­ing Yi tells us more about this work:

In many ver­teb­rates, sex is determ­ined genet­ic­ally by a pair of sex chro­mo­somes (e.g., XY in males and XX in females). Sex chro­mo­somes have been found to con­trib­ute to repro­duct­ive bar­ri­er and even pro­mote spe­ci­ation. There­fore, pop­u­la­tions hav­ing dif­fer­ent sex chro­mo­somes are usu­ally expec­ted to not hybrid­ize very well. How­ever, in the nine-spined stickle­back (Pun­gi­ti­us pun­gi­ti­us), pop­u­la­tions in west­ern and east­ern Europe hybrid­ize in the Balt­ic Sea des­pite hav­ing dif­fer­ent pairs of sex chro­mo­somes. Yet it has remained unknown how dif­fer­ent sex chro­mo­somes are sor­ted out in these hybrid populations.

Pre­vi­ous stud­ies have shown that east­ern European pop­u­la­tions and ances­tral non-European pop­u­la­tions have mor­pho­lo­gic­ally dif­fer­ent (i.e., het­ero­morph­ic) X and Y chro­mo­somes iden­ti­fied as the link­age group 12 (LG12). How­ever, LG12 is not asso­ci­ated with sex in west­ern European pop­u­la­tions whose sex chro­mo­somes are mor­pho­lo­gic­ally sim­il­ar (i.e., homo­morph­ic) and remained unidentified.

In this recently pub­lished study, we iden­ti­fied LG3 as the homo­morph­ic X and Y chro­mo­somes in most west­ern European pop­u­la­tions, except for the UK pop­u­la­tions which seem to have a poten­tially dif­fer­ent sex-determ­in­ing sys­tem. The sex-determ­in­ing region of LG3 is very short (~80 kbp) com­pared to that of LG12 (~16.9 Mbp), which is expec­ted giv­en the lack of mor­pho­lo­gic­al dif­fer­en­ti­ation between LG3 X and Y chro­mo­somes and their rel­at­ively short­er evol­u­tion­ary time. Inter­est­ingly, an inver­sion was indic­ated in the sex-determ­in­ing region of the LG3 Y chro­mo­some. Because inver­sions pre­vent chro­mo­some recom­bin­a­tion in their sur­round­ing regions, they might con­trib­ute to the form­a­tion of sex-determ­in­ing regions in the early evol­u­tion of sex chromosomes.

With both west­ern and east­ern sex chro­mo­somes iden­ti­fied, we attemp­ted to sort out how nine-spined stickle­backs hav­ing dif­fer­ent sex chro­mo­somes hybrid­ize in their con­tact zone. We iden­ti­fied the genet­ic sex of 887 wild-caught indi­vidu­als from 45 glob­ally dis­trib­uted pop­u­la­tions. Almost all pop­u­la­tions were iden­ti­fied with only one pair of sex chro­mo­somes (i.e., LG12, LG3, or unknown in UK), includ­ing the admixed mar­ine pop­u­la­tion in Ger­many where only LG3-determ­ined males were iden­ti­fied. How­ever, the highly admixed pop­u­la­tion in Poland was iden­ti­fied with both pairs of sex chro­mo­somes but in a skewed ratio, includ­ing 10 LG3-determ­ined males and one LG12-determ­ined male. Genet­ic ana­lyses using auto­somes showed that this single LG12-determ­ined male is not a migrant from more east­ern pop­u­la­tions. In addi­tion, the skewed ratio of LG3 versus LG12 sex chro­mo­somes could not be explained by sex-spe­cif­ic gene flow between west­ern and east­ern populations.

There­fore, the over-rep­res­ent­a­tion of LG3-determ­ined males in the hybrid zone indic­ates rel­at­ively lower fit­ness of the LG12-detemined males in this region. This sug­gests that there might be an ongo­ing trans­ition of sex chro­mo­somes (i.e., sex chro­mo­some turnover) in the hybrid zone where the homo­morph­ic LG3 appears to take over the het­ero­morph­ic LG12 as sex chromosomes.

Our study thus provides an empir­ic­al example to show that hybrid­iz­a­tion between lin­eages hav­ing dif­fer­ent sex chro­mo­somes can trig­ger sex chro­mo­some turnover in the hybrid zone. The dir­ec­tion of this turnover is con­sist­ent with the hypo­thes­is of selec­tion against high­er dele­ter­i­ous muta­tion loads accu­mu­lated on evol­u­tion­ar­ily older and het­ero­morph­ic sex chro­mo­somes. Altern­at­ively, the LG3 sex chro­mo­somes might be favored by selec­tion in the hybrid zone due to poten­tial link­age with bene­fi­cial genes. Addi­tion­al research is needed to test these altern­at­ive hypo­theses and demon­strate the mech­an­isms that drive sex chro­mo­some turnovers.

This study intro­duces more ques­tions that await to be answered in future work. For example, what are the sex chro­mo­somes in the UK pop­u­la­tions? How did the LG3 Y chro­mo­some evolve and how was the poten­tial inver­sion involved? Are there any incom­pat­ib­il­it­ies between west­ern and east­ern lin­eages? If so, are those incom­pat­ib­il­it­ies related to dif­fer­ent sex chro­mo­somes? Answer­ing these ques­tions in nine-spined stickle­backs will also con­trib­ute to our over­all under­stand­ing of sex chro­mo­some evol­u­tion and diversity.

Dr. Xuel­ing Yi is a postdoc­tor­al schol­ar in the Mer­ilä Lab at the Uni­ver­sity of Hong Kong. The ori­gin­al art­icle is freely avail­able to read and down­load from Evol­u­tion Letters.