Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat

Mendoza, Marie Lisandra Zepeda; Xiong, Zijun; Escalera-Zamudio, Marina; Runge, Anne Kathrine Wiborg; Thézé, Julien; Streicker, Daniel G.; Frank, Hannah K.; Loza-Rubio, Elizabeth; Liu, Shengmao; Ryder, Oliver A.; Castruita, José Alfredo Samaniego; Katzourakis, Aris; Pacheco, George; Taboada, Blanca; Löber, Ulrike; Pybus, Oliver G.; Yang, Li V.; Rojas-Anaya, Edith; Bohmann, Kristine; Baez, Aldo Carmona; Arias, Carlos F.; Liu, Shiping; Greenwood, Alex D.; Bertelsen, Mads F.; White, Nicole E.; Bunce, Michael; Zhang, Guojie; Sicheritz-Pontén, Thomas; Gilbert, M. Thomas P.

doi:10.1038/s41559-018-0476-8

Cited by 129 publications

(151 citation statements)

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“…This composition is consistent with previous reports of vampire bat microbiotas (Carrillo-Araujo et al, 2015;Ingala et al, 2018;Phillips et al, 2012). Vampire bats have gut microbiotas that are compositionally distinct from those of other bats, most likely as a result of selective pressures to optimize bacterial metabolism of bloodmeals (Zepeda Mendoza et al, 2018). Indeed, vampire bats share several key hemolytic bacterial symbionts, such as Aeromonas spp., with other blood-feeding animals such as leeches (Muller, Pinus, & Schmidt, 1980), suggesting that hematophagous animal microbiome composition is closely associated with this specialized diet.…”

Section: Discussionsupporting

confidence: 91%

“…Future studies using shotgun metagenomic techniques could be used to analyze how the microbiota changes on a gene-by-gene basis in response to habitat quality, which may give more detailed insight to how these changes in vampire bats impact metagenome functions related to immunity. For example, a hologenomic study of vampire bats found that their microbiotas were characterized by an enrichment of potentially protective bacterial genes originating from Amycolatopsis mediterranei, which is known to produce antiviral compounds (Zepeda Mendoza et al, 2018). Expansion of our study (a) across a quantitative fragmentation gradient and (b) using shotgun metagenomic techniques could provide detailed insights into the functional consequences of habitat fragmentation on vampire bat microbiotas.…”

Section: Discussionmentioning

confidence: 89%

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Habitat fragmentation is associated with dietary shifts and microbiota variability in common vampire bats

Ingala

Becker

Holm

et al. 2019

Ecology and Evolution

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Host ecological factors and external environmental factors are known to influence the structure of gut microbial communities, but few studies have examined the impacts of environmental changes on microbiotas in free‐ranging animals. Rapid land‐use change has the potential to shift gut microbial communities in wildlife through exposure to novel bacteria and/or by changing the availability or quality of local food resources. The consequences of such changes to host health and fitness remain unknown and may have important implications for pathogen spillover between humans and wildlife. To better understand the consequences of land‐use change on wildlife microbiotas, we analyzed long‐term dietary trends, gut microbiota composition, and innate immune function in common vampire bats (Desmodus rotundus) in two nearby sites in Belize that vary in landscape structure. We found that vampire bats living in a small forest fragment had more homogenous diets indicative of feeding on livestock and shifts in microbiota heterogeneity, but not overall composition, compared to those living in an intact forest reserve. We also found that irrespective of sampling site, vampire bats which consumed relatively more livestock showed shifts in some core bacteria compared with vampire bats which consumed relatively less livestock. The relative abundance of some core microbiota members was associated with innate immune function, suggesting that future research should consider the role of the host microbiota in immune defense and its relationship to zoonotic infection dynamics. We suggest that subsequent homogenization of diet and habitat loss through livestock rearing in the Neotropics may lead to disruption to the microbiota that could have downstream impacts on host immunity and cross‐species pathogen transmission.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 89%

Habitat fragmentation is associated with dietary shifts and microbiota variability in common vampire bats

Ingala

Becker

Holm

et al. 2019

Ecology and Evolution

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“…For OPN1SW, we obtained sequence data for 28 species from the transcriptome data sets. We then supplemented the OPN1SW nucleotide sequences with those extracted from genome data using a combination of blastn and bl2seq on five noctilionoid bat genomes (Artibeus jamaicensis, Desmodus rotundus (Zepeda Mendoza et al, 2018), Lionycteris spurrelli, Macrotus waterhousii, Mormoops blainvillei and Noctilio leporinus) using the Miniopterus natalensis OPN1SW (XM_016213323.1) sequence as a query. The L. spurrelli and M. waterhousii genomes were sequenced by the Rossiter Lab, and the A. jamaicensis, M. blainvillei and N. leporinus genomes were made available by the Broad Institute.…”

Section: Ihc -Photoreceptor Quantificationmentioning

confidence: 99%

“…Opsin gene evolution We used aligned sequences from the transcriptomes of 38 species together 429 with those from six noctilionoid genomes (Zepeda Mendoza et al, 2018) to estimate rates of 430 molecular evolution of visual opsin genes (OPN1SW, OPN1LW, and RHO) in focal bats. First, we 431 tested for divergent selection modes among species that had S-opsin cones, lacked the S-opsin 432 cones but had an intact mRNA sequence, and those that lacked the S-opsin cones but either did 433 not have OPN1SW transcripts or had a pseudogenized OPN1SW sequence (Figure supplement 2) 434 using the Branch Model 2 of codeml in PAML 4.8a (Yang, 2007).…”

mentioning

confidence: 99%

Evidence for multifactorial processes underlying phenotypic variation in bat visual opsins

Sadier

Davies

Yohe

et al. 2018

Preprint

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27Studies of opsin genes offer insights into the evolutionary history and molecular basis of vertebrate 28 color vision, but most assume intact open reading frames equate to functional phenotypes. Despite 29 known variation in opsin repertoires and associated visual phenotypes, the genetic basis of such 30 patterns has not been examined at each step of the central dogma. By comparing sequences, gene 31 expression, and protein localization across a hyperdiverse group of mammals, noctilionoid bats, 32we find evidence that independent losses of S-opsin arose through disruptions at different stages 33 of protein synthesis, while maintenance relates to frugivory. Discordance between DNA, RNA, 34 and protein reveals that the loss of short-wave sensitivity in some lineages resulted from 35 transcriptional and post-transcriptional changes in addition to degradation of open reading frames. 36These mismatches imply that visual phenotypes cannot reliably be predicted from genotypes alone, 37 and connect ecology to multiple mechanisms behind the loss of color in vertebrates. 38 39 Introduction 40

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“…Although still poorly studied in bats, the gut microbiota could be another factor related to their high digestion efficiency (Zepeda Mendoza et al. ). Bats have different gut microbial communities depending whether they feed on fruits, nectar, blood, or insects (Phillips et al.…”

Section: Resultsmentioning

confidence: 99%

Ecology and evolutionary biology of fishing bats

Aizpurua

Alberdi

2018

Mammal Review

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A few of the >1300 bat species recognised worldwide are known to consume fish to various extents. However, empirical information about how and how much different bat species capture and consume fish is limited and is probably distorted due to the biases introduced by occasional observations. In this review, we aim to synthesise the knowledge so far generated on fishing bats, in order to 1) assess the incidence of fishing in different bat species; 2) discuss the evolutionary framework and origins of fishing behaviour; and 3) identify the ecological challenges of fishing and review the state of knowledge about kinetic, morphological, sensory, behavioural, and physiological adaptations related to fishing. Fishing bats can be clustered into three groups based on the incidence of fish consumption. Noctilio leporinus is the only species in which fishing is widespread (occurring in most populations) and common (occurring most of the time and carried out by many individuals). Myotis vivesi, Myotis pilosus, and Myotis capaccinii comprise the second group, characterised by exhibiting regular fishing behaviour that is restricted to a limited number of populations. Noctilio albiventris, Myotis daubentonii, and Myotis macropus are classified in a third group, because although the occasional presence of fish traces in faeces has been reported, regular fishing behaviour in the wild has not been confirmed. Fishing was developed independently multiple times in different bat lineages, probably under different selective pressures and ecological scenarios. Nevertheless, all fishing species face similar challenges in terms of detecting, capturing, handling, and metabolising fish, which require specific kinetic, morphological, sensory, behavioural, and physiological adaptations. Both basic information about fishing behaviour in different species and specific knowledge of the biological adaptation are still missing. Thus, in this review we identify gaps in the knowledge and suggest experimental approaches to overcome them.

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Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat

Cited by 129 publications

References 91 publications

Habitat fragmentation is associated with dietary shifts and microbiota variability in common vampire bats

Habitat fragmentation is associated with dietary shifts and microbiota variability in common vampire bats

Evidence for multifactorial processes underlying phenotypic variation in bat visual opsins

Ecology and evolutionary biology of fishing bats

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