Dietary Diversification and Specialization in Neotropical Bats Facilitated by Early Molecular Evolution

Abstract

Dietary adaptation is a major feature of phenotypic and ecological diversification, yet the genetic basis of dietary shifts is poorly understood. Among mammals, Neotropical leaf-nosed bats (family Phyllostomidae) show unmatched diversity in diet; from a putative insectivorous ancestor, phyllostomids have radiated to specialize on diverse food sources, including blood, nectar, and fruit. To assess whether dietary diversification in this group was accompanied by molecular adaptations for changing metabolic demands, we sequenced 89 transcriptomes across 58 species, and combined these with published data to compare ∼13,000 protein coding genes across 66 species. We tested for positive selection on focal lineages, including those inferred to have undergone dietary shifts. Unexpectedly, we found a broad signature of positive selection in the ancestral phyllostomid branch, spanning genes implicated in the metabolism of all major macronutrients, yet few positively selected genes at the inferred switch to plantivory. Branches corresponding to blood- and nectar-based diets showed selection in loci underpinning nitrogenous waste excretion and glycolysis, respectively. Intriguingly, patterns of selection in metabolism genes were mirrored by those in loci implicated in craniofacial remodelling, a trait previously linked to phyllostomid dietary specialisation. Finally, using simulations, we show that the widely-used branch-site model is likely to be misspecified, with the implication that it is too conservative and probably under-reports true cases of positive selection. Our findings point to a complex picture of adaptive radiation, in which the evolution of new dietary specialisations has been facilitated by early adaptations combined with the generation of new genetic variation.

Nectar-feeding bats and birds show parallel molecular adaptations in sugar metabolism enzymes

“…Analyses of bats and birds were conducted separately with bat-or bird-only alignments, in each case examining one focal lineage while removing other nectar feeders from the background set of taxa. Our results yielded 219 candidate positively selected genes (PSGs; p < 0.05) in Glossophaginae (branch-site, 144; clade, 77; Data S2A and S2B), which included branch-site loci reported previously; 11 269 in Lonchophyllinae (branch-site, 239; clade, 33; Data S2C and S2D); 141 in Eonycteris (branch-site only; Data S2E); and 661 in Trochilidae (branch-site, 622; clade, 45; Data S2G and S2H).…”

“…[41][42][43][44][45][46][47][48][49][50] We also used additional bat transcriptomes from published SRA data. 11,41,50,51 Our final dataset comprised 126 mammal and bird species, including 25 nectar-feeders (Data S1C).…”

Positive selection drives the evolution of a primate bitter taste receptor gene

“…The positive selection imposed on EC regions could be attributed to their involvement in tastant recognition, while acknowledging that with certain still need further functional assay. Moreover, some problems with inferences of positive selection based on comparing the models implemented in PAML have been identified, and admittedly most of these problems have been found in tests that involve branch-site models (Potter et al, 2021;Venkat et al, 2018), but it is not clear how they may translate to the site models. Thus, it is suggested that caution should be taken when we draw conclusions from models comparison by using PAML software package.…”

Long-read sequencing reveals rapid evolution of immunity- and cancer-related genes in bats

“…However, we also tested for positive selection on the lineages leading to each of the two newly sequenced bats. Observing a highly skewed distribution of nominal p-values (p>0.98 in 86% of tests), we opted to follow a recent study 56 and omit a correction for multiple comparisons across orthologs, instead adjusting only for testing on three different branches (but see Table S10 and Data S1 for more conservative adjusted p-values). Based on this strategy, we identified 468 positively selected genes (PSGs) with adjusted p<0.05 in the bat MRCA (Figure 3, Table S10).…”