Determining the Null Model for Detecting Adaptive Convergence from Genomic Data: A Case Study using Echolocating Mammals

Abstract

Convergent evolution occurs when the same trait arises independently in multiple lineages. In most cases of phenotypic convergence such transitions are adaptive, so finding the underlying molecular causes of convergence can provide insight into the process of adaptation. Convergent evolution at the genomic level also lends itself to study by comparative methods, although molecular convergence can also occur by chance, adding noise to this process. Parker et al. studied convergence across the genomes of several mammals, including echolocating bats and dolphins (Parker J, Tsagkogeorga G, Cotton JA, Liu Y, Provero P, Stupka E, Rossiter SJ. 2013. Genome-wide signatures of convergent evolution in echolocating mammals. Nature 502:228-231). On the basis of a null distribution of site-specific likelihood support (SSLS) generated using simulated topologies, they concluded that there was evidence for genome-wide adaptive convergence between echolocating taxa. Here, we demonstrate that methods based on SSLS do not adequately measure convergence, and reiterate the use of an empirical null model that directly compares convergent substitutions between all pairs of species. We find that when the proper comparisons are made there is no surprising excess of convergence between echolocating mammals, even in sensory genes.

Keywords: adaptation; convergence; echolocation; parallel evolution.

Fig. 1.

Convergence between echolocating species does not exceed expectations. (a) The phylogenetic relationships among the mammal species studied here. Echolocating species are shown in boxes. (b) The number of convergent and divergent substitutions along external branches of the tree between all pairs of nine mammal species. The correlation (R² = 0.88) between these types of substitutions provides an appropriate expectation for convergence (Castoe et al. 2009). The circled dots represent comparisons of interest between microbat–dolphin and microbat–cow. The three dots at the bottom of the panel represent sister-taxon comparisons, for which it is nearly impossible to infer convergent changes (such comparisons were excluded from Castoe et al. 2009).

Fig. 2.

Convergent substitutions between both microbat–dolphin and microbat–cow. (a) Of the 1,372 genes found with convergent changes between microbat and dolphin, 738 also had convergent changes between microbat and the nonecholocating cow. (b) The number of genes with multiple convergent substitutions in comparisons between microbat–dolphin and microbat–cow. Sensory genes with convergent substitutions are assigned to their corresponding bin indicating the number of convergent substitutions they contain in either comparison. Genes with stars next to their name have convergent substitutions in both comparisons. There are 22 sensory genes in each comparison, indicating no surprising convergence between echolocators.