Parallel genetic changes underlie integrated craniofacial traits in an adaptive radiation of trophic specialist pupfishes

Abstract

Many factors such as divergence time, shared standing genetic variation, frequency of introgression, and mutation rates can influence the likelihood of whether populations adapt to similar environments via parallel or non-parallel genetic changes. However, the frequency of parallel vs non-parallel genetic changes resulting in phenotypic convergence is still rarely estimated. In this study, we used a QTL mapping approach to investigate the genetic basis of highly divergent craniofacial traits between scale- and snail-eating trophic specialist species across similar hypersaline lake environments in an adaptive radiation of pupfishes endemic to San Salvador Island, Bahamas. We raised F2 intercrosses of scale- and snail-eaters from two different lake populations of sympatric specialists, estimated linkage maps, and scanned for significant QTL for 30 skeletal craniofacial and body traits. We then compared the location of QTL in each lake for each trait to determine whether convergence in this system is due primarily to parallel or non-parallel genetic changes. We found strong support for parallel genetic changes in both lakes for five traits in which we detected a significant QTL in at least one lake. However, many of these shared QTL affected different, but highly correlated craniofacial traits in each lake, suggesting that pleiotropy and trait integration should not be neglected when estimating rates of parallel evolution.We also found that shared QTL regions between lakes were six times more likely to contain at least one highly differenciated variant under selection in wild pupfish populations than the rest of the genome. We further observed a 23-52% increase in adaptive introgression within shared QTL, suggesting that introgression may be important for parallel evolution. Overall, our results suggest that the same genomic regions contribute to the convergent phenotypes of snail- and scale-eating across lakes, and that those genomic regions contain more introgressed adaptive alleles than expected by chance. We also highlight the need for more expansive searches for shared QTL when testing for parallel evolution.

Competing Interest Statement

The authors have declared no competing interest.