Parallel and Convergent Evolution of the Dim-Light Vision Gene RH1 in Bats (Order: Chiroptera)

Abstract

Rhodopsin, encoded by the gene Rhodopsin (RH1), is extremely sensitive to light, and is responsible for dim-light vision. Bats are nocturnal mammals that inhabit poor light environments. Megabats (Old-World fruit bats) generally have well-developed eyes, while microbats (insectivorous bats) have developed echolocation and in general their eyes were degraded, however, dramatic differences in the eyes, and their reliance on vision, exist in this group. In this study, we examined the rod opsin gene (RH1), and compared its evolution to that of two cone opsin genes (SWS1 and M/LWS). While phylogenetic reconstruction with the cone opsin genes SWS1 and M/LWS generated a species tree in accord with expectations, the RH1 gene tree united Pteropodidae (Old-World fruit bats) and Yangochiroptera, with very high bootstrap values, suggesting the possibility of convergent evolution. The hypothesis of convergent evolution was further supported when nonsynonymous sites or amino acid sequences were used to construct phylogenies. Reconstructed RH1 sequences at internal nodes of the bat species phylogeny showed that: (1) Old-World fruit bats share an amino acid change (S270G) with the tomb bat; (2) Miniopterus share two amino acid changes (V104I, M183L) with Rhinolophoidea; (3) the amino acid replacement I123V occurred independently on four branches, and the replacements L99M, L266V and I286V occurred each on two branches. The multiple parallel amino acid replacements that occurred in the evolution of bat RH1 suggest the possibility of multiple convergences of their ecological specialization (i.e., various photic environments) during adaptation for the nocturnal lifestyle, and suggest that further attention is needed on the study of the ecology and behavior of bats.

Nuclear organization of cholinergic, putative catecholaminergic and serotonergic systems in the brains of two megachiropteran species

“…These other microbat families have a lower average body temperature because of torpor and may not have joined megachiropterans and rhinolophoids because their DNA is less modified in consequence (Pettigrew and Kirsch, 1998). Studies have recently appeared using DNA sequences that question the megachiropteran-rhinolophoid link (Shen et al, 2010;Li et al, 2008). Moreover, protein sequence data from the same genes used for DNA studies also fail to support the megabat-rhinolophoid association and instead provide evidence in favour of the flying primate hypothesis (e.g.…”

“…These include Dictyostelium, a eucaryote which DNA analysis places with the procaryotes (Loomis and Smith, 1990), Amphioxus, a cephalochordate that is placed outside the echinoderms by DNA analysis (Naylor and Brown, 1998), and megachiropterans and rhinolophoids which spuriously associate unless their DNA is corrected for a base compositional bias resulting from high metabolic rate (Pettigrew and Kirsch, 1998). In these examples, DNA convergence was detected and corrected using conflict between the DNA tree and the protein tree of the same gene, a common occurrence in bats compared to other mammals (Shen et al, 2010;Li et al, 2007). In view of the claims for convergence on both sides of the debate about the phylogeny of chiropterans, an overall contextual view seems necessary, as opposed to one based upon a single approach.…”

Hippocampal Neurogenesis and Cortical Cellular Plasticity in Wahlberg’s Epauletted Fruit Bat: A Qualitative and Quantitative Study

“…However, hippocampal neurogenesis in microbats was observed to be largely absent and, when present, occurred at a low rate [Amrein et al, 2007]. Microbats and the non-echolocating fruit bats (Megachiroptera) share an evolutionary history with a unique adaptation to flight and longevity [Teeling et al, 2000;Shen et al, 2010;Wilkinson and South, 2002]. Fruit bats use olfactory and visual senses for spatial orientation and navigation [Hodgkison et al, 2007;Raghuram et al, 2009] and indeed, brain regions processing visual and olfactory information are proportionally larger in fruit bats compared to insectivore bats [Barton et al, 1995;Hutcheon et al, 2002].…”

Photic niche invasions: phylogenetic history of the dim-light foraging augochlorine bees (Halictidae)

“…Parallel and convergent evolution has been identified in the rhodopsin gene of bats [54]. In augochlorine bees, the non-photic gene matrix (EF1-a and Wg) did not group the dim-light lineages within a single clade, but the alternate paraphyletic arrangement was not statistically supported (electronic supplementary material, figure S2).…”