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Pilot Fecal DNA Barcoding on Selected Fruit Bats in Davao City, Philippines

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Pilot Fecal DNA Barcoding on Selected Fruit Bats in Davao City, Philippines Philippine Journal of Science 150 (2): 545-555, April 2021 ISSN 0031 - 7683 Date Received: 17 Sep 2020 Pilot Fecal DNA Barcoding on Selected Fruit Bats in Davao City, Philippines Michael G. Bacus2, Sammer C. Burgos1, Hannah G. Elizagaque1, Kameela Monique A. Malbog1, Mae A. Responte1,3, Lief Erikson D. Gamalo1,2,3, Marion John Michael M. Achondo1,3, and Lyre Anni E. Murao1,2,3* 1Department of Biological Sciences and Environmental Studies 2Philippine Genome Center Mindanao 3Wildlife-Human Interaction Studies, Ecological Research and Biodiversity Conservation Laboratory University of the Philippines Mindanao, Mintal Davao City, Region XI 8000 Philippines The “Species from Feces” DNA barcoding offers new opportunities to study the challenging taxonomy and systematics of Philippine bats using a minimally-invasive strategy that employs a short 200- bp mitochondrial encoded cytochrome c oxidase I (mt COI) sequence. A pilot application of the technique to five species of fruit bats collected from Davao City, Philippines revealed accurate species identification and the extended ability to assess genetic diversity and evolutionary relationships. The 95–100% sequence identity matched with the field identification of bats, including the endemic Ptenochirus jagori, although only 62% of the samples could be sequenced. A decreasing trend in genetic diversity was noted from widespread bat species such as Rousettus amplexicaudatus, Cynopterus brachyotis, and Macroglossus minimus to species with limited geographic distribution (e .g . P . jagori) or possible recent colonization (e .g . Eonycteris spelaea). Genetic diversity, principal coordinate analysis (PCoA), and phylogenetic analysis also showed distinct genetic lineages of C . brachyotis, R . amplexicaudatus, and M . minimus from their conspecifics outside the Philippines, while E . spelaea and the endemic P . jagori exhibited genetic homogeneity. The findings on genetic diversity and relationships were consistent with previous studies using longer COI segment or other biomarkers. In conclusion, the Species from Feces DNA barcoding presents a minimally invasive and pragmatic approach to explore bat assemblages with the additional utility to examine genetic structures and relationships, which may be used to support studies on diversity, evolution, and biogeography, thereby rapidly facilitate conservation initiatives. Keywords: evolution, fecal barcoding, fruit bats, genetic diversity INTRODUCTION 2018; Heaney et al. 2005; Ingle and Heaney 1992). Among these species, 32% are estimated to be under the family Bats (Order: Chiroptera) are one of the most diverse and Pteropodidae, which are the fruit- or nectar-feeding bats widely distributed groups of mammals. Around 1,386 (Tanalgo and Hughes 2018). Although members of this species of bats exist around the world, of which around family share some unique ecological features (e.g. only 70 species are present in the Philippines (Burgin et al. eat plant matter, most do not echolocate), they differ *Corresponding Author: [email protected] from each other in terms of habitat preference, roosting 545 Philippine Journal of Science Bacus et al.: Fecal DNA Barcoding on Selected Vol. 150 No. 2, April 2021 Philippine Fruit Bats habits, and aggregation sizes (Heaney et al. 2016). Some between conspecifics, thus making it an efficient tool for genera of the family are also endemic in the country (e.g. species identification (Hebert et al. 2003). Analysis of 165 Haplonycteris and Ptenochirus), which is an evidence bat species in Southeast Asia revealed that DNA barcoding of the rich and enormous evolutionary diversification of using the mt COI gene could effectively discriminate bats within the archipelago (Heaney et al. 2005; Heaney between morphologically or acoustically distinct et al. 2016). species, except for some closely related species such as Macroglossus minimus (É. Geoffroy Saint-Hilaire, 1810) Bats provide numerous ecosystem services such as vs. Macroglossus sobrinus K. Andersen, 1911, Cynopterus pollination, seed dispersal, and pest suppression (Kunz et horsfieldii Gray, 1843 vs. Cynopterus brachyotis Müller, al. 2011). They are also indicators for biodiversity due to 1838, Rhinolophus macrotis Blyth, 1844 vs. Rhinolophus their critical role in maintaining ecosystem health (Jones et siamensis Gyldenstolpe, 1917, and Myotis annamiticus al. 2009). These underscore the importance of monitoring Kruskop and Tsytsulina, 2001 vs. Myotis laniger Peters, bat populations to yield appropriate management decisions 1871 (Francis et al. 2010). and strategies for chiropteran conservation (Russo and Voigt 2016). However, the first taxonomic key of bats Non-invasive approaches for obtaining genetic samples in the Philippines that was developed in 1992 has not are safer for bats and make genetic techniques more been updated since then, resulting in huge gaps in the accessible to researchers. Non-lethal strategies to obtain establishment of definitive taxonomic and systematics bat DNA include hair and wing punches (Pfunder et records in the Philippines (Tanalgo and Hughes 2018). al. 2004). Recently, a DNA mini-barcode assay called Species from Feces was developed for bat identification Bat identification is typically based on morphological from guano or fecal pellets obtained from abandoned traits, which often requires capturing bats manually mines used by bats in Arizona, Colorado, New Mexico, or through traps (i.e. mist nets, harp nets, etc.). Due to and Utah in the United States of America (USA) using their small size, morphological identification demands a 202-bp segment, which overlaps with the standard careful examination and occasional misidentification ~ 500-bp barcode from the mt COI-5P region used may occur (Francis 1989; Francis et al. 2010). This is in the Barcode of Life Database or BOLD (Walker further complicated by sympatric and morphologically et al. 2016). Evaluation of the assay in tissues and similar species, which may be difficult to distinguish feces of 54 chiropteran species from eight bat families (Lim et al. 2017). In many cases, confirmation requires (Pteropodidae, Rhinolophidae, Rhinopomatidae, morphometric analysis of the skull and dentition with Molossidae, Mormoopidae, Noctilionidae, reference to published materials (Francis et al. 2010) Phyllostomidae, and Vespertilionidae) validated its and through acoustic devices (Russo and Voigt 2016). effectiveness to discriminate between species. The assay Hence, identification of bats in the field can be extremely was also confirmed to be bat-specific since arthropod challenging while collection of voucher specimens is prey was not detected using next-generation sequencing delimited by government and ethical restrictions (Wilson platforms. Although the assay has been recommended et al. 2014). for individual (single feces) or community (guano or DNA barcoding has an important application for pooled feces) analysis of bat populations, its utility in conservation as proper inventory of species is critical for Philippine bats has not been demonstrated. This study is assigning the appropriate units and scales in conservation a pilot demonstration of minimally invasive molecular planning (Francis et al. 2010). DNA barcode markers can profiling of selected Philippine fruit bats from Davao also be used to extract information on genetic diversity City using fecal matter based on the mt COI gene. and relatedness of populations, and even discover new species for the purposes of conservation planning (Francis et al. 2010; Wilson et al. 2014). Additional strategies with a more comprehensive approach for barcoding are MATERIALS AND METHODS needed for a concise and robust distinction of population relatedness and genetic structure. Sampling Two sampling sites in Davao City, Philippines were DNA barcoding has been recently introduced as another selected for this study – Mintal (7.0854° N, 125.4864° approach to bat identification, with the mt COI gene as E) and Malagos (7.1876° N, 125.4289° E). Sampling was the most commonly used marker to distinguish between conducted at 18:00–5:00 for five days in May–July 2017 species as has been demonstrated for 20 bat species in and two days in November 2018 for Mintal and Malagos, the Phyllostomidae family and 19 bat species in the respectively. Bats were collected through convenience Pteropodidae family (Hernandez-Davila et al. 2012; sampling using mist nets, and the morphometric Luczon et al. 2019). Its sequence is also conserved characteristics were measured such as total length, 546 Philippine Journal of Science Bacus et al.: Fecal DNA Barcoding on Selected Vol. 150 No. 2, April 2021 Philippine Fruit Bats forearm length, tail length, and ear length. A preliminary Sequence Analysis identification was given according to their morphometric The sequences were cleaned and edited using FinchTV characteristics using the taxonomic key developed by software (Geospiza, Inc.) and a contig sequence was Ingle and Heaney (1992) (Appendix Table I). Bats were generated from the forward and reverse sequences temporarily placed in clean muslin bags until defecation using BioEdit (Ibis Biosciences, California, USA) (Hall and were released after a maximum possible amount of 1999). The Basic Local Alignment Search Tool (BLAST) fecal sample was collected. In Malagos, non-endemic from NCBI (http://www.ncbi.nlm.nih.gov/) and BOLD and non-threatened species were anesthetized through (biodiversitygenomics.net/projects/bold) were used for intraperitoneal injection of tiletamine-zolazepam
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