Genetic and evolutionary consequences of range expansion revealed

A new study pub­lished in Evol­u­tion Let­ters exam­ines how mat­ing sys­tems have been shaped by his­tor­ic biogeo­graph­ic events. Lead author Matt Koski explains the find­ings and what they tell us about evol­u­tion­ary responses to glob­al cli­mate change.

His­tor­ic cli­mate oscil­la­tions have been a driv­ing force in shap­ing the geo­graph­ic dis­tri­bu­tion of spe­cies. Dur­ing the last ice age, many plants and anim­als were restric­ted to suit­able hab­it­at called gla­cial refu­gia. In the North­ern Hemi­sphere these refu­gia often exis­ted at south­erly lat­it­udes. As the glob­al cli­mate warmed and gla­ciers receded pole­ward, spe­cies expan­ded out of these refu­gia into newly suit­able hab­it­at.  Pick­ing up and mov­ing to a new loc­a­tion should have import­ant impacts on the genet­ic diversity of pop­u­la­tions, their evol­u­tion, and maybe even their fate. Do we find a leg­acy of his­tor­ic range expan­sion in con­tem­por­ary pop­u­la­tions and does this provide insight into poten­tial responses to con­tem­por­ary cli­mate change?

Col­on­iz­a­tion of new hab­it­ats often involves just a few indi­vidu­als, res­ult­ing in reduced genet­ic diversity rel­at­ive to source pop­u­la­tions. Repeated founder events dur­ing range expan­sion should there­fore reduce diversity in pop­u­la­tions farthest from gla­cial refu­gia. Anoth­er genet­ic con­sequence of range expan­sion can be the accu­mu­la­tion and fix­a­tion of harm­ful muta­tions in pop­u­la­tions at the expand­ing range edge. This is called the ‘expan­sion load’ and it can reduce the fit­ness of pop­u­la­tions near expand­ing edges. Geo­graph­ic range expan­sion should also have cas­cad­ing effects on a fun­da­ment­al aspect of repro­duc­tion in herm­aph­rod­it­ic organ­isms — wheth­er to find a mate (out­cross) or mate with them­selves (self-fer­til­ize). In small found­ing pop­u­la­tions, indi­vidu­als that are able to self-fer­til­ize may be favored because they don’t need to find a mate to repro­duce. Addi­tion­ally, in pop­u­la­tions with low genet­ic diversity (like those far from gla­cial refu­gia) rare harm­ful muta­tions that reduce the per­form­ance of inbred off­spring may be lost through founder events. These ideas both sug­gest that self-fer­til­iz­a­tion evolves more eas­ily in pop­u­la­tions with low genet­ic diversity.

To test for these con­sequences of range expan­sion, we stud­ied pop­u­la­tions across the geo­graph­ic range of Amer­ic­an bell­flower (Cam­pan­ula amer­ic­ana)—a cha­ris­mat­ic flower­ing plant from east­ern North Amer­ica (Fig. 1).

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Fig­ure 1: A flower of Cam­pan­ula amer­ic­ana being vis­ited by a halict­id bee. 

An import­ant first step in this work was to fig­ure out where the spe­cies likely hid out dur­ing peri­ods of gla­ci­ation. We had sev­er­al ideas giv­en past work in this spe­cies, but we wanted to fully lever­age our gen­om­ic data. We ended up bor­row­ing a tech­nique taken from anoth­er dis­cip­line (the “time dif­fer­ence of arrival” approach, which can be used to solve some nav­ig­a­tion prob­lems).  Using this meth­od, we ana­lyzed the geo­graph­ic dis­tri­bu­tion of derived alleles to estab­lish that the most likely ori­gin of range expan­sion (i.e., the gla­cial refu­gi­um) was in the South­ern Appalachi­ans in present-day south­east­ern Ken­tucky (Fig. 2A). Pop­u­la­tions farther from this point were effect­ively smal­ler (Fig. 2B), reflect­ing a his­tory of bot­tle­necks. Such a find­ing is expec­ted whenev­er the expand­ing range edge is pushed for­ward by the move­ment of few indi­vidu­als again and again through time.

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Fig­ure 2: (A) The most likely loc­a­tion of the gla­cial refu­gi­um (‘x’) for 24 focal pop­u­la­tions of C. amer­ic­ana west of the Appalachi­an moun­tains. (B) Genet­ic diversity declines with dis­tance from the refugium.

After we estab­lished the loc­a­tion of a gla­cial refu­gi­um, we then inter­preted genet­ic dif­fer­ences among pop­u­la­tions in this light. We found that pop­u­la­tions at the expand­ing range edge also dis­played reduced fit­ness when crossed with mem­bers of their own pop­u­la­tion rel­at­ive to cross­ing with oth­er pop­u­la­tions. This was the phen­o­typ­ic expres­sion of muta­tion accu­mu­la­tion and reduced genet­ic diversity at the expand­ing edge. Thus, the expan­sion load depressed aver­age pop­u­la­tion fitness.

We then turned our atten­tion to geo­graph­ic vari­ation in the abil­ity to self-fer­til­ize among pop­u­la­tions, or their abil­ity to pro­duce fruit in the absence of pol­lin­at­ors. Autonom­ous fruit set was very tightly linked with both the dis­tance from the gla­cial refu­gi­um and genet­ic drift load (Fig. 3). That is, pop­u­la­tions that col­on­ized farther from the gla­cial refu­gi­um have an elev­ated abil­ity to self-fer­til­ize. This res­ult strongly implies that range expan­sion has struc­tured geo­graph­ic vari­ation of the mat­ing sys­tem. Pre­vi­ous work found that pol­lin­at­or activ­ity and the num­ber of plants in a pop­u­la­tion (i.e., mate avail­ab­il­ity) were unre­lated to autonom­ous self­ing abil­ity in Amer­ic­an bell­flower. Thus, his­tor­ic­al pro­cesses shaped vari­ation in the poten­tial for self­ing, but this may not neces­sar­ily be adapt­ive in con­tem­por­ary populations.

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Fig­ure 3: Autonom­ous fruit set increases with (A) the dis­tance from the gla­cial refu­gi­um and (B) drift load. 

In the end, does this work in bell­flower change the way we think about evol­u­tion? We think it draws atten­tion to older his­tor­ic­al events as determ­in­ants of plant sexu­al sys­tems. Since the middle of the 20th cen­tury, a wealth of stud­ies that have shed import­ant light on why plants out­cross or self. While the eco­logy of con­tem­por­ary pop­u­la­tions (e.g., mate avail­ab­il­ity, or pol­lin­at­or avail­ab­il­ity) is clearly import­ant, our bell­flower study shows that his­tor­ic col­on­iz­a­tion can explain much vari­ation in the geo­graphy of plant repro­duc­tion. In an even broad­er per­spect­ive, this work high­lights some of the poten­tial costs of range expan­sion that are likely to haunt spe­cies that move into new hab­it­ats made suit­able by warm­ing cli­mates. Muta­tion accu­mu­la­tion has the poten­tial to restrict spe­cies’ ranges and lim­it adapt­a­tion to con­tem­por­ary cli­mate change. Our work only hints at these pos­sib­il­it­ies. Future work in evol­u­tion­ary bio­logy will of course see wheth­er these ideas stand the test of time.

 

Matt Koski is Assist­ant Pro­fess­or at the Depart­ment of Bio­lo­gic­al Sci­ences, Clem­son Uni­ver­sity. The ori­gin­al study is freely avail­able to read and down­load from Evol­u­tion Letters.