skip to main content


Title: Complete mitochondrial genomes reveal robust phylogenetic signals and evidence of positive selection in horseshoe bats
Abstract Background In genus Rhinolophus , species in the Rhinolophus philippinensis and R. macrotis groups are unique because the horseshoe bats in these group have relatively low echolocation frequencies and flight speeds compared with other horseshoe bats with similar body size. The different characteristics among bat species suggest particular evolutionary processes may have occurred in this genus. To study the adaptive evidence in the mitochondrial genomes (mitogenomes) of rhinolophids, especially the mitogenomes of the species with low echolocation frequencies, we sequenced eight mitogenomes and used them for comparative studies of molecular phylogeny and adaptive evolution. Results Phylogenetic analysis using whole mitogenome sequences produced robust results and provided phylogenetic signals that were better than those obtained using single genes. The results supported the recent establishment of the separate macrotis group. The signals of adaptive evolution discovered in the Rhinolophus species were tested for some of the codons in two genes ( ND2 and ND6 ) that encode NADH dehydrogenases in oxidative phosphorylation system complex I. These genes have a background of widespread purifying selection. Signals of relaxed purifying selection and positive selection were found in ND2 and ND6 , respectively, based on codon models and physicochemical profiles of amino acid replacements. However, no pronounced overlap was found for non-synonymous sites in the mitogenomes of all the species with low echolocation frequencies. A signal of positive selection for ND5 was found in the branch-site model when R. philippinensis was set as the foreground branch. Conclusions The mitogenomes provided robust phylogenetic signals that were much more informative than the signals obtained using single mitochondrial genes. Two mitochondrial genes that encoding proteins in the oxidative phosphorylation system showed some evidence of adaptive evolution in genus Rhinolophus and the positive selection signals were tested for ND5 in R. philippinensis . These results indicate that mitochondrial protein-coding genes were targets of adaptive evolution during the evolution of Rhinolophus species, which might have contributed to a diverse range of acoustic adaptations in this genus.  more » « less
Award ID(s):
1911853
NSF-PAR ID:
10336871
Author(s) / Creator(s):
; ; ; ; ; ;
Date Published:
Journal Name:
BMC Ecology and Evolution
Volume:
21
Issue:
1
ISSN:
2730-7182
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. In the process of species differentiation and adaption, the relative influence of natural selection on gene expression variation often remains unclear (especially its impact on phenotypic divergence). In this study, we used differentially expressed genes from brain, cochlea, and liver samples collected from two species of bats to determine the gene expression variation forced by natural selection when comparing at the interspecific (Rhinolophus siamensis and R. episcopus episcopus) and the intraspecific (R. e. episcopus and R. episcopus spp.) levels. In both cases, gene expression variation was extensively adaptive (>66.0%) and mainly governed by directional selection, followed by stabilizing selection, and finally balancing selection. The expression variation related to acoustic signals (resting frequency, RF) and body size (forearm length, FA) was also widely governed by natural selection (>69.1%). Different functional patterns of RF- or FA-related adaptive expression variation were found between the two comparisons, which manifested as abundant immune-related regulations between subspecies (indicating a relationship between immune response and phenotypic adaption). Our study verifies the extensive adaptive expression variation between both species and subspecies and provides insight into the effects of natural selection on species differentiation and adaptation as well as phenotypic divergence at the expression level. 
    more » « less
  2. Tully, Damien (Ed.)
    Virus host shifts are generally associated with novel adaptations to exploit the cells of the new host species optimally. Surprisingly, Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) has apparently required little to no significant adaptation to humans since the start of the Coronavirus Disease 2019 (COVID-19) pandemic and to October 2020. Here we assess the types of natural selection taking place in Sarbecoviruses in horseshoe bats versus the early SARS-CoV-2 evolution in humans. While there is moderate evidence of diversifying positive selection in SARS-CoV-2 in humans, it is limited to the early phase of the pandemic, and purifying selection is much weaker in SARS-CoV-2 than in related bat Sarbecoviruses . In contrast, our analysis detects evidence for significant positive episodic diversifying selection acting at the base of the bat virus lineage SARS-CoV-2 emerged from, accompanied by an adaptive depletion in CpG composition presumed to be linked to the action of antiviral mechanisms in these ancestral bat hosts. The closest bat virus to SARS-CoV-2, RmYN02 (sharing an ancestor about 1976), is a recombinant with a structure that includes differential CpG content in Spike; clear evidence of coinfection and evolution in bats without involvement of other species. While an undiscovered “facilitating” intermediate species cannot be discounted, collectively, our results support the progenitor of SARS-CoV-2 being capable of efficient human–human transmission as a consequence of its adaptive evolutionary history in bats, not humans, which created a relatively generalist virus. 
    more » « less
  3. Abstract

    Successful reproduction depends on interactions between numerous proteins beyond those involved directly in gamete fusion. Although such reproductive proteins evolve in response to sexual selection pressures, how networks of interacting proteins arise and evolve as reproductive phenotypes change remains an open question. Here, we investigated the molecular evolution of the ‘sex peptide network’ ofDrosophila melanogaster,a functionally well‐characterized reproductive protein network. In this species, the peptide hormone sex peptide (SP) and its interacting proteins cause major changes in female physiology and behaviour after mating. In contrast, females of more distantly relatedDrosophilaspecies do not respond to SP. In spite of these phenotypic differences, we detected orthologs of all network proteins across 22 diverseDrosophilaspecies and found evidence that most orthologs likely function in reproduction throughout the genus. Within SP‐responsive species, we detected the recurrent, adaptive evolution of several network proteins, consistent with sexual selection acting to continually refine network function. We also found some evidence for adaptive evolution of several proteins along two specific phylogenetic lineages that correspond with increased expression of the SP receptor in female reproductive tracts or increased sperm length, respectively. Finally, we used gene expression profiling to examine the likely degree of functional conservation of the paralogs of an SP network protein that arose via gene duplication. Our results suggest a dynamic history for the SP network in which network members arose before the onset of robust SP‐mediated responses and then were shaped by both purifying and positive selection.

     
    more » « less
  4. Abstract

    Sensory systems perform fitness‐relevant functions, and specialized sensory structures allow organisms to accomplish challenging tasks. However, broad comparative analyses of sensory morphologies and their performance are lacking for diverse mammalian radiations.

    Neotropical leaf‐nosed bats (Phyllostomidae) are one of the most ecologically diverse mammal groups; including a wide range of diets and foraging behaviours, and extreme morphological variation in external sensory structures used in echolocation (nose leaf and pinnae).

    We coupled 3D geometric morphometrics and acoustic field recordings under a phylogenetic framework to investigate the mechanisms underlying the diversification of external sensory morphologies in phyllostomids, and explored the potential implications of sensory morphological diversity to functional outputs and dietary ecology.

    We found that the nose leaf consists of two evolutionary modules—spear and horseshoe—suggesting that modularity enabled morphological and functional diversification of this structure.

    We found a significant association between some aspects of nose leaf shape and maximum frequency and bandwidth of echolocation calls, but not between pinnae shape and echolocation call parameters. This may be explained by the use of multiple sensory modes across phyllostomids and plasticity of some echolocation call parameters.

    Species with different diets significantly differed in nose leaf shape, specifically in spear breadth, presence of a midrib, and cupping and anterior rotation of the horseshoe. This may relate to different levels of prey type specificity within each diet. Pinnae shape significantly differed between species that consume non‐mobile, non‐evasive prey (broad rounded, cupped pinnae) and mobile, evasive prey (flattened pinnae with a sharp tapering apex). This may reflect the use of different sound cues to detect prey.

    Our results give insight into the morphological evolution of external sensory structures in bats, and highlight new links between morphological diversity and ecology.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less
  5. Abstract

    Changes in behaviour may initiate shifts to new adaptive zones, with physical adaptations for novel environments evolving later. While new mutations are commonly considered engines of adaptive change, sensory evolution enabling access to new resources might also arise from standing genetic diversity, and even gene loss. We examine the relative contribution of molecular adaptations, measured by positive and relaxed selection, acting on eye‐expressed genes associated with shifts to new adaptive zones in ecologically diverse bats from the superfamily Noctilionoidea. Collectively, noctilionoids display remarkable ecological breadth, from highly divergent echolocation to flight strategies linked to specialized insectivory, the parallel evolution of diverse plant‐based diets (e.g., nectar, pollen and fruit) from ancestral insectivory, and—unusually for echolocating bats—often have large, well‐developed eyes. We report contrasting levels of positive selection in genes associated with the development, maintenance and scope of visual function, tracing back to the origins of noctilionoids and Phyllostomidae (the bat family with most dietary diversity), instead of during shifts to novel diets. Generalized plant visiting was not associated with exceptional molecular adaptation, and exploration of these novel niches took place in an ancestral phyllostomid genetic background. In contrast, evidence for positive selection in vision genes was found at subsequent shifts to either nectarivory or frugivory. Thus, neotropical noctilionoids that use visual cues for identifying food and roosts, as well as for orientation, were effectively preadapted, with subsequent molecular adaptations in nectar‐feeding lineages and the subfamily Stenodermatinae of fig‐eating bats fine‐tuning pre‐existing visual adaptations for specialized purposes.

     
    more » « less