Evolution of an adaptive behavior and its sensory receptors promotes eye regression in blind cavefish: response to Borowsky (2013)

Vibration attraction behavior (VAB) is the swimming of fish toward an oscillating object, a behavior that is likely adaptive because it increases foraging efficiency in darkness. VAB is seen in a small proportion of Astyanax surface-dwelling populations (surface fish) but is pronounced in cave-dwelling populations (cavefish). In a recent study, we identified two quantitative trait loci for VAB on Astyanax linkage groups 2 and 17. We also demonstrated that a small population of superficial neuromast sensors located within the eye orbit (EO SN) facilitate VAB, and two quantitative trait loci (QTL) were identified for EO SN that were congruent with those for VAB. Finally, we showed that both VAB and EO SN are negatively correlated with eye size, and that two (of several) QTL for eye size overlap VAB and EO SN QTLs. From these results, we concluded that the adaptive evolution of VAB and EO SN has contributed to the indirect loss of eyes in cavefish, either as a result of pleiotropy or tight physical linkage of the mutations underlying these traits. In a subsequent commentary, Borowsky argues that there is poor experimental support for our conclusions. Specifically, Borowsky states that: (1) linkage groups (LGs) 2 and 17 harbor QTL for many traits and, therefore, no evidence exists for an exclusive interaction among the overlapping VAB, EO SN and eye size QTL; (2) some of the QTL we identified are too broad (>20 cM) to support the hypothesis of correlated evolution due to pleiotropy or hitchhiking; and (3) VAB is unnecessary to explain the indirect evolution of eye-loss since the negative polarity of numerous eye QTL is consistent with direct selection against eyes. Borowsky further argues that (4) it is difficult to envision an evolutionary scenario whereby VAB and EO SN drive eye loss, since the eyes must first be reduced in order to increase the number of EO SN and, therefore, VAB. In this response, we explain why the evidence of one trait influencing eye reduction is stronger for VAB than other traits, and provide further support for a scenario whereby elaboration of VAB in surface fish may precede complete eye-loss.