Colour vision variation in leaf‐nosed bats (Phyllostomidae): Links to cave roosting and dietary specialization

Abstract

Bats are a diverse radiation of mammals of enduring interest for understanding the evolution of sensory specialization. Colour vision variation among species has previously been linked to roosting preferences and echolocation form in the suborder Yinpterochiroptera, yet questions remain about the roles of diet and habitat in shaping bat visual ecology. We sequenced OPN1SW and OPN1LW opsin genes for 20 species of leaf-nosed bats (family Phyllostomidae; suborder Yangochiroptera) with diverse roosting and dietary ecologies, along with one vespertilionid species (Myotis lavali). OPN1LW genes appear intact for all species, and predicted spectral tuning of long-wavelength opsins varied among lineages. OPN1SW genes appear intact and under purifying selection for Myotis lavali and most phyllostomid bats, with two exceptions: (a) We found evidence of ancient OPN1SW pseudogenization in the vampire bat lineage, and loss-of-function mutations in all three species of extant vampire bats; (b) we additionally found a recent, independently derived OPN1SW pseudogene in Lonchophylla mordax, a cave-roosting species. These mutations in leaf-nosed bats are independent of the OPN1SW pseudogenization events previously reported in Yinpterochiropterans. Therefore, the evolution of monochromacy (complete colour blindness) has occurred in both suborders of bats and under various evolutionary drivers; we find independent support for the hypothesis that obligate cave roosting drives colour vision loss. We additionally suggest that haematophagous dietary specialization and corresponding selection on nonvisual senses led to loss of colour vision through evolutionary sensory trade-off. Our results underscore the evolutionary plasticity of opsins among nocturnal mammals.

Multifactorial processes underlie parallel opsin loss in neotropical bats

“…Weight of branches indicates: inferred presence of protein – heavy; inferred absence of protein – light; protein absence based on evidence of gene loss but not confirmed by IHC – dashed light. We were either not able to recover mRNA, or preserved material was not available, for species marked with ‘*’, evidence for ORF status for Diaemus youngi taken from Kries et al, 2018. The species phylogeny follows Rojas et al, 2016 and Shi and Rabosky, 2015.…”

“…Emerling et al, 2015, Emerling et al, 2017, Hunt and Peichl, 2014, Kraus et al, 2014 and Zhao et al, 2009a), including bats from both suborders (e.g. Emerling et al, 2015, Kim et al, 2008, Kries et al, 2018, Müller et al, 2007, Wu et al, 2018 and Zhao et al, 2009a). In general, pseudogenization is thought to occur relatively frequently within mammalian genomes, and previous estimates suggest several thousand pseudogenes may be present per genome (e.g.…”

“…However, with increased taxonomic sampling of neotropical bat species this has been shown to not be the case, and multiple independent lineages with diverse ecologies (e.g. blood feeding, plant-visiting species) show evidence of OPN1SW pseudogenization (Kries et al, 2018; Li et al, 2018; Wu et al, 2018). Notably, lineages shown to have lost their S-opsins – and thus by association UV-sensitivity – are from the Noctilionoidea superfamily.…”

“…Similarly, while the taxonomic sampling of the recent studies of neotropical bat vision (e.g. Gutierrez et al, 2018, Kries et al, 2018, Li et al, 2018, and Wu et al, 2018) is considerably more extensive than previous work, it remains limited, and the functionality of OPN1SW has been based on analyses of DNA sequences and a few transcriptome samples.…”

Foraging shifts and visual preadaptation in ecologically diverse bats

“…(commonly known as big‐eyed bats) (Eklöf, 2003; Thiagavel et al., 2018). Despite this, molecular ecology studies of noctilionoid vision have thus far been limited to visual opsins ( OPN1SW , OPN1LW and RHO ), and traced adaptations therein to changes in roosting habits, echolocation and diets (Kries et al., 2018; Li et al., 2018; Sadier et al., 2018; Simões et al., 2019; Wu, Jiao, Simmons, Lu, & Zhao, 2018). Additional analyses correlated foraging modes (e.g., aerial vs. gleaning insectivory) and visual evolution by contrasting selection intensity between two sets of species with divergent foraging ecologies, but were again restricted to the opsins (Gutierrez, Schott, et al, 2018).…”