dna barcodes reveal high genetic diversity in philippine fruit bats · 2019. 10. 9. · keywords:...

Keywords: COI gene, cryptic species, DNA barcoding, Pteropodidae

DNA Barcodes Reveal High Genetic Diversity in Philippine Fruit Bats

1Institute of Biology, College of Science, University of the Philippines, Diliman, Quezon City 1101 Philippines

2Rizal Medical Center, Pasig Blvd., Barangay Bagong Ilog Pasig City 1600 Philippines3Philippine Genome Center, University of the Philippines

Diliman, Quezon City 1101 Philippines

Adrian U. Luczon1*, Sofia Anne Marie M. Ampo1,2, John Gregor A. Roño1, Mariano Roy M. Duya1, Perry S. Ong1, and Ian Kendrich C. Fontanilla1,3

Fruit bats of the family Pteropodidae is the third largest family in the order Chiroptera. There are 26 recorded species in the Philippines, 17 of which are endemic to the country. However, the number of species in the archipelago may still be underestimated. With the growing threats to biodiversity and dwindling number of taxonomists, DNA barcodes can assist with the problem by providing an accurate, rapid, and effective method of species recognition. To contribute to the barcoding endeavor and determine the diversity of Philippine fruit bats, a 542-base-pair portion of the cytochrome c oxidase subunit 1 (COI) gene was sequenced from 111 individuals belonging to 19 pteropodid species. A neighbor-joining (NJ) and maximum likelihood (ML) tree was generated using the sequences in this study and other available sequences in Genbank and Barcode of Life Data Systems (BOLD). DNA barcodes were effective in delineating Philippine species. Closer inspection of the NJ tree revealed distinct [> 6% mean Kimura-2-parameter (K2P) distance] Philippine lineages for Macroglossus minimus, Rousettus amplexicaudatus, Megaerops wetmorei, and Cynopterus brachyotis relative to conspecifics from Southeast Asia. Between-island differentiation was also observed for the Philippine endemic Haplonycteris fischeri (> 7% mean between-island K2P distance). From this study, these species may be flagged for taxonomic reevaluation.

Philippine Journal of Science148 (S1): 133-140, Special Issue on GenomicsISSN 0031 - 7683Date Received: 18 Mar 2019

*Corresponding Author: [email protected]

INTRODUCTIONThe catalog of mammalian species found in the Philippine archipelago is far from complete. Just recently, 28 new species of non-volant mammals were discovered by Heaney et al. (2016a). Certainly, more species can still be discovered, especially in remote and unexplored parts of the archipelago (Heaney et al. 2010). Species with cryptic morphology and habits may also contribute to the number of overlooked taxa, a common occurrence in bats

(Campbell et al. 2004, Galimberti et al. 2010). Looking at Vespertilionidae, Phyllostomidae, and Pteropodidae – the three largest families of bats – the number of recognized species in 2005 were 407, 160, and 186, respectively (Simmons 2005). However, based on the latest record in 2017 (ASM 2019), the number of species increased considerably (Vespertiolionidae, 24.07%; Phyllostomidae, 35%; and Pteropodidae 5.4%).

Nevertheless, species are still endangered throughout the world and in the Philippines through activities such as habitat disturbance and overharvesting of animals (Francis

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et al. 2010). Globally, a quarter of the total mammalian species is threatened with extinction, and half have declining populations (Myers et al. 2000). Conservation measures must therefore be put in place to maintain the local biodiversity, and proper steps cannot be taken unless species are correctly identified.

As the number of classically trained taxonomists is dwindling (Hebert et al. 2003), a molecular method for identifying species known as DNA barcoding is gaining increasing importance as source of data for taxonomy. DNA barcoding uses a standard region of the genome as a genetic marker for identifying species. In animals, the 5’ end of the COI is the DNA barcode of choice. Although the task of identifying and describing new species is ultimately achieved through comprehensive taxonomic work, DNA barcoding and the data derived from it can significantly facilitate the process by serving as a supplement to the identification provided by morphological taxonomists (Hajibabaei et al. 2007). It can also facilitate the “democratization” of taxonomic knowledge by making expert taxonomic information available to non-experts in an applied context (Holloway 2006).

As DNA sequences have become the major source of new information for advancing understanding of evolutionary and genetic relationships (Hajibabaei et al. 2007), the data obtained in this study may contribute substantially to current knowledge on chiropteran classification. In the same way, DNA barcode libraries can serve as effective identification systems for any regional bat fauna (Clare et al. 2007). DNA barcode analysis and the methodology it employs can be applied in a standardized manner across large domains of life – overcoming the difficulty presented by conventional taxonomy, where multiple data types may be required, depending on the taxa being studied (Hajibabaei et al. 2007). Use of DNA barcodes translates to more species being examined in a shorter span of time with less cost. The profiles obtained from barcodes will be cost-effective in many taxonomic contexts. It is important to acknowledge that, at present, access to this new technology is not always readily available to everyone. Nevertheless, innovations in sequencing technology promise future reductions in the cost of DNA-based identifications (Hebert et al. 2003). DNA barcoding may also serve as the basis for a global bioidentification system for animals that will overcome the deficiencies of morphological approaches to species discrimination and allow single laboratories to execute taxon diagnoses across the full spectrum of animal life (Hebert et al. 2003). However, genetic differentiation has its limitations as it cannot incorporate the fossil record or older museum specimens with degraded material. A database of COI profiles coupled with other data (images, geographic location, and other specimen data) can also serve as a

robust record gathered by morphological taxonomists (Hebert et al. 2003).

The family of fruit bats, Pteropodidae, is one of the largest bat families within the order Chiroptera having around 45 genera and about 196 recognized species (ASM 2019). In the Philippines, there are about 26 recognized species (Tanalgo and Hughes 2018) – 17 of which (about 65%) are endemic to the country.

COI barcodes for native and endemic Philippine fruit bat species are lacking. To contribute to current published barcoding data for pteropodids, the study aims to obtain sequences of the COI gene of the fruit bats in the Philippines. The study also aims to test the viability of the marker in delineating the new COI records from existing pteropodids in the database. A gene tree for Philippine bats and those in existing databases were constructed to assess the fruit bat species diversity in the archipelago based on COI. The study will not only be able to document DNA diversity of bats but also have practical applications such as in wildlife forensics.

MATERIALS AND METHODSSampling

Fruit bats were collected from 17 sites in the Philippines (see Figure 1). Samples used in this study came from various collections by the authors, as well as collections by other researchers mentioned in the acknowledgments.

Figure 1. Map showing the collection sites of specimens in this study.

Special Issue on Genomics Luczon et al.: DNA barcoding of Philippine fruit bats

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Species identification was based on Ingle and Heaney (1992). Tissue samples collected came in the form of 2-mm wing punches from individuals that were captured and released, or muscle from vouchered specimens. Tissues collected were kept frozen or placed in a microcentrifuge tube with 95–100% ethanol. At least three individuals per species were used for the study.

DNA Extraction, PCR Amplification, and Sequencing Genomic DNA was obtained from the tissues using the Promega™ Wizard® SV Genomic DNA Purification Kit (USA) following the manufacturer’s protocols. The COI gene was amplified using the primers VF1 (TTCTCAACCAACCACAARGAYATYGG) and VR1 (TAGACTTCTGGGTGGCCRAARAAYCA) (Ivanova et al. 2006). Alternatively, the mammal primer cocktail (Ivanova et al. 2012) was used for other specimens. A 30-μL reaction mix was prepared using the genomic DNA, primers, and Taq dNTPack (Roche, USA). The PCR reaction consisted of 5 μL 10x polymerase chain reaction (PCR) reaction buffer with 15 mM Mg2+, 1 μL 1.25 mM dNTP mix, 10 μL Q buffer, 1 μL 25 mM MgCl2, 2.5 μL of 10 mM each of forward and reverse primers, 27.85 μL distilled water, 0.25 μL of 5 units/μL Taq polymerase, and 2.4 μL of approximately 20 ng/μL DNA sample. PCR amplification was done in a Labnet MultiGene™ thermocycler under the following conditions: one cycle initial denaturation at 94 °C for 2 min; five cycles of 94 °C for 40 s, 45 °C for 45 s, and 72 °C for 1.5 min; 35 cycles of 94 °C for 40 s, 51 °C for 45 s, and 72 °C for 1.5 min; and a final extension at 72 °C for 5 min.

The PCR products were run on a 1% agarose gel and visualized using EtBr-UV illumination. Bands formed in the gel were excised and purified using QIAquick® DNA Extraction Kit (Qiagen, USA) following the manufacturer’s protocols. The purified products were sent to 1st BASE Pte. Ltd. in Malaysia or Macrogen Inc. in South Korea for DNA sequencing.

Sequence AnalysisSequences provided by the service providers were assembled using the Staden Package (Staden et al. 2000). Sequences and other data were uploaded to BOLD (Process IDs BPHB092-16 – BPHB127-16, BPHB133-18 – BPHB158-18, BPHP159-19 – BPHP207-19) and Genbank (Accession numbers MK585711 – MK585812, MK622922 - MK622930). BOLD records are publicly available under the dataset DS-PHPTERO (dx.doi.org/10.5883/DS-PTERODS). To see how the COI sequences generated from this study cluster with COI sequences of other species, COI sequences of pteropodid bats from GenBank and the BOLD were included in the analysis. Finally, three individuals from the family Rhinolophidae – a sister family based on the study of

Almeida et al. (2011) – was included as an outgroup in the final data set. The list of specimens in this study can be found in Appendix I, while the list of sequences from Genbank and BOLD used in the dataset can be found in Appendix II.

The dataset was then aligned using MAFFT version 7 (Katoh et al. 2017), followed by manual alignment as needed. The lengths of sequences were made uniform to 542 base pairs to accommodate sequences that were shorter in length. The complete dataset included 817 sequences, of which 111 are pteropodid sequences generated from this study.

MEGA 7 (Kumar et al. 2016) was used to calculate pairwise K2P distances needed to construct a COI gene tree. An NJ tree (Nei and Saitou 1987) with 1000 bootstrap replicates was constructed to view the groupings of the sequences. An ML tree using RaxML (Stamatakis 2014) with 1000 bootstraps (rapid bootstrap algorithm) and a best-fit model of substitution acquired from jModelTest 2 (Darriba et al. 2012) was also constructed to see if there is an alternative grouping for this study’s generated sequences. The substitution model GTR plus gamma and proportion of invariant sites (GTR+G+I) was selected as the best-fit model of substitution based on the Akaike Information Criterion (Akaike 1973).

RESULTSThis study was able to generate 111 DNA barcodes, representing 19 of the 26 known Philippine pteropodid species. Of these species, 13 are new species records for the COI region. In addition, all generated barcodes are new pteropodid records from the Philippines.

Figures 2 and 3 are the NJ and ML gene trees, respectively, that were generated from the COI data set. Overall, mean intraspecific genetic K2P distance is significantly lower than interspecific and intergeneric distances (Table 1). However, overlaps between the ranges of these categories were observed. In particular, some interspecific and intergeneric pairwise distances exhibited small values (< 3% pairwise distance). Examples of these cases are pairwise distances between the species Micropteropus pusillus and Epomophorous gambianus, Pteropus lylei and Pteropus vampyrus, and Macroglossus minimus and Macroglossus sobrinus from Genbank and BOLD. These cases where DNA barcodes fail to distinguish species have been observed and discussed in other studies (Francis et al. 2010, Nesi et al. 2011).

The topologies of the NJ and ML are vastly different at the internal nodes of the trees. However, there is general agreement between them regarding the groupings of the generated sequences at the terminal nodes. On one case, however, NJ and ML disagreed on the position of


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Macroglossus minimus. In the NJ tree, M. minimus in the Philippines (PH) forms a separate clade from the M. minimus / M. sobrinus clade from other Southeast Asian (SEA) countries (bootstrap = 99%). However, the ML tree places M. minimus PH within the M. minimus / M. sobrinus

Figure 2. COI NJ tree for Pteropodidae dataset using K2P model of substitution. Bootstrap supports 50% or greater are shown in the nodes. Clades with more than one sequence have been compressed. Labels indicate scientific name and number of sequences for that taxon in the clade. Red lines indicate Philippine pteropodid sequences generated in this study. Scientific names in bold text indicate known Philippine endemic species. Colored shapes indicate the geographic origin of the sequences from Genbank and BOLD: purple – Southeast Asia, red – East Asia, blue – South Asia, white – Middle East, yellow – Africa, and black – Oceania. Scale indicates two nucleotide substitutions per 100 nucleotides.

Figure 3. COI ML tree for Pteropodidae dataset using GTR+G+I model of substitution. Bootstrap supports 50% or greater are shown in the nodes. Clades with more than one sequence have been compressed. Labels indicate scientific name and number of sequences for that taxon in the clade. Scientific names in bold text indicate known Philippine endemic species. Colored shapes indicate the geographic origin of the sequences from Genbank and BOLD: purple – Southeast Asia, red – East Asia, blue – South Asia, white – Middle East, yellow – Africa, and black – Oceania. Red lines indicate sequences generated by this study. Scale indicates five nucleotide substitutions per 100 nucleotides.

SEA clade (bootstrap = 100%). Upon closer inspection of the ML tree, it is apparent that the M. minimus / M. sobrinus SEA is distinct from M. minimus PH (Figure 4).

Most of the species collected in the Philippines show barcode sequences that are unique. Only sequences of


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Eonycteris spelaea and Pteropus hypomelanus generated in this study have nested within their respective conspecifics in BOLD and Genbank. For the rest of the species, COI sequences generated in this study formed distinct lineages. The 13 new species barcodes each formed distinct and well-supported clades in the trees (NJ bootstrap = 99%, ML bootstrap = 83–100%) and therefore show that COI is effective in identifying them as separate species.

Results also show that COI sequences can be used to delineate Philippine fruit bat species from their conspecific counterparts in Asia. For example, as previously mentioned, Philippine lineages of M. minimus are distinct from the M. minimus / M. sobrinus clade from other SEA countries. Between the two groups, a high K2P distance of 6.63% was observed. The same can be said for Rousettus amplexicaudatus where the Philippine clade has a mean K2P distance of 12.75% from its SEA counterpart. Sequences of Megaerops wetmorei generated in this study did not group with its congenerics. Instead, the group was observed to be a sister clade of the Ptenochirus and Cynopterus. Lastly, it was observed that C. brachyotis sequences did not form a monophyletic group. Instead, the Philippine lineage was distinct from the SEA lineage (mean K2P distance = 11.45%) and both formed a species complex with C. horsfieldii and C. sphinx (see Table 1).

Interisland variations were observed for the endemic Haplonycteris fischeri. In the NJ and ML trees, the species split into three groups that represent the specimens collected from mainland Luzon, Mindoro Island, and Mindanao Island. On average, these three lineages had an interisland K2P distance of 7.50% (range: 6.67–8.30%), which indicates that COI was able to detect genetically distinct populations for this taxon.

Figure 4. Sub-tree of the M. minimus / M. sobrinus clade from Figure 3 showing the Philippine clade (red line) and Southeast Asian clade (black line). Scale indicates five nucleotides substitutions per 1000 nucleotides.

Table 1. Summary of pairwise genetic distance at different categories: PH – sequences generated in this study, SEA – sequences from Southeast Asia available in Genbank and BOLD.

Pairwise category Mean distance (%) Minimum (%) Maximum (%)

Overall intraspecific distance 1.39 0 16.2

Overall interspecific distance 19.87 0 27.10

Overall intergeneric distance 20.36 0 27.10

M. minimus PH vs. SEA 6.63 6.00 7.60

R. amplexicaudatus PH vs. SEA 12.75 11.20 13.50

C. brachyotis PH vs. SEA 11.45 9.60 12.80

M. wetmorei PH vs. SEA 16.20 16.20 16.20

H. fischeri Mindoro vs. Mindanao islands 7.17 6.90 7.50

H. fischeri Mindoro vs. Luzon islands 7.80 7.10 8.30

H. fischeri Mindanao vs. Luzon islands 7.29 6.70 8.00


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DISCUSSIONThis study provides the first records of Philippine barcodes of the family Pteropodidae and is a complement to previous efforts on DNA barcoding of pteropodid bats within Southeast Asia (Francis et al. 2010).

Results in this study show that the COI barcode is effective in distinguishing fruit bat species. DNA barcoding relies on the capability of a standard genetic marker to distinguish between species. A marker of choice must be able to separate intraspecific variation and interspecific divergence for it to accurately differentiate between species (Meyer and Paulay 2005). The COI gene can ideally distinguish between closely related species – even between haplotypes and geographic variants – owing to a high rate of evolution that easily produces divergent sequences (Hebert et al. 2003, Clare et al. 2007, Francis et al. 2010).

Both the NJ and ML trees show well-supported clades for the sequences generated in this study. Moreover, they generally agree with each other in terms of the groupings at the terminal nodes of the trees, which is important for the objectives of DNA barcoding. In the case of the discordance between the NJ and ML trees with regards to the placement of M. minimus PH, it was observed that sequences of the group had a relatively higher mutation rate than the rest of the M. minimus sequences. In addition, all sequences still clustered together and formed a distinct lineage. Overall, the use of NJ trees with K2P distances is sufficient in delineating species, at least for Philippine fruit bats in our dataset.

Past studies have revealed high diversity and endemicity of bats through DNA barcodes (Clare et al. 2007, Francis et al. 2010). This study supports this idea for the Philippine species as can be observed for the lineages of the new records and in Philippine lineages of C. brachyotis, M. minimus, M. wetmorei, and R. amplexicaudatus. The high endemicity and diversity in the Philippine archipelago can be attributed to its unique geological history (Heaney and Roberts 2009, Heaney et al. 2016b).

The distinct Philippine lineage of C. brachyotis has been documented in a previous study. Based on cytochrome b and control region sequences, Campbell et al. (2004) noted the presence of a species complex across the range of C. brachyotis. Their study observed at least six distinct lineages in Southeast Asia, one of which is in the Philippines. This and our study lend support to the reassignment of C. brachyotis to C. luzoniensis (Peters, 1861).

Rookmaaker and Bergmans (1981) suggested three subspecies under R. amplexicaudatus based on morphology – R. a. amplexicaudatus (Geoffroy, 1810); R. a. infumatus (Gray 1870); and R. a. brachyotis (Dobson 1877). R.

amplexicaudatus in the Philippines was assigned to R. a. amplexicaudatus together with populations from mainland Southeast Asia, Borneo, Timor, Maluku, and Papua New Guinea. However, the high K2P distance (12.70%) between the PH clade and SEA clade seems to indicate cryptic speciation for R. amplexicaudatus in the country. Similarly, M. minimus PH, which is traditionally placed under M. minimus lagochilus (Maryanto and Kitchener 1999), is distinct from other members of the subspecies. In the case of M. wetmorei, the divergence of the Philippine samples from the one M. wetmorei sample from Malaysia (Genbank accession number = HM540878) may reflect subspecies divergence between M. w. wetmorei (where Philippine species belong) and M. w. albicolis (Francis 1989). Future studies should sample across the biogeographic ranges of these species and use more markers to be able to clarify the taxonomic status of the Philippine lineages.

In the case of the endemic H. fischeri, three distinct island lineages were observed. This result agrees with the study of Roberts (2006) regarding the diversity of H. fischeri. In their study, cytochrome b and ND2 sequences revealed divergence of this species between islands. The presence of a unique lineage in each Pleistocene island complex (Brown and Diesmos 2002) gives evidence to how the configuration of the Philippine archipelago during this geologic time period influenced the splitting of these lineages.

Most of the barcodes for pteropodid species in the Philippines represent distinct COI lineages. However, these unique lineages must be studied further to confirm if they are indeed a different species. Using single mitochondrial gene is prone to bias, usually against recently diverged or currently diverging species and taxa whose reproductive isolation times are highly variable, lending possibility to the underestimation of diversity of the taxon being studied (Song et al. 2008). Introgression – the repeated backcrossing of existing hybrids – is also known to interfere with the resolution of relationships using a single gene (Hickerson et al. 2006). Indeed, the value of DNA barcoding is to flag species in need of taxonomic revision and perform more robust analyses (Hajibabaei et al. 2007). In future studies, it is prudent to use more genetic markers and to sample across the whole species range in order to be more precise in estimating the diversity of a species. If substantial evidence has been gathered to prove that a species within a certain geographic range is a different species or – at the very least – a unique genetic lineage, governments and conservation organizations such as CITES must recognize these species as a separate conservation unit, and therefore requires its own resource for conservation efforts.


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CONCLUSIONDNA barcoding is an important tool, not only in identifying species, but also in discovering putative new species. Barcoding of Philippine pteropodids reveal many distinct lineages, some of which may need taxonomic reevaluation based on the results of this study. For future studies, barcodes of other pteropodid species are important to obtain to complete the Philippine database for pteropodids. Additionally, the use of more robust molecular markers for phylogeny and/or morphological studies can be done on the species that were flagged in this study.

ACKNOWLEDGMENTSWe are grateful for the following agencies that funded our work: Emerging Science & Technology program and the Emerging Interdisciplinary Research of the Office of the Vice President for Academic Affairs – University of the Philippines System (EIDR-C06-022.4), the Department of Science and Technology, Energy Development Corporation, Commission on Higher Education, Biodiversity Management Bureau of the Department of Environment and Natural Resources, Forest Global Earth Observatory (previously known as Center for Tropical Forest Science), the Field Museum of Natural History, and USAID Protect Wildlife. We are also grateful for the Biodiversity Research Lab of the Institute of Biology, University of the Philippines Diliman; Holistic Education and Development Center; Ms. Maria Nina Regina Quibod; and Dr. Lawrence Heaney and the Field Museum for Natural History for providing some of the samples.

STATEMENT ON CONFLICT OF INTERESTThe authors have no conflict of interest to declare.

NOTES ON APPENDICES The complete appendices section of the study is accessible at http://philjournsci.dost.gov.ph

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Table I. List of specimens collected in this study.Species BOLD process ID Genbank Accession # Location of collection

Acerodon jubatus BPHB198-19 MK585769 Dona Remedios Trinidad, Bulacan

BPHB126-16 MK585751 Castilla, Sorsogon

Alionycteris paucidentata BPHB134-18 MK585756 Bukidnon

BPHB135-18 MK585798 Bukidnon


Cynopterus brachyotis BPHB173-19 MK585783 Occidental Mindoro

BPHB189-19 MK585759 Palanan, Isabela


BPHB138-18 MK585743 Siquijor

BPHB136-18 MK585722 Kalinga

BPHB172-19 MK585753 Magsaysay, Occidental Mindoro


BPHB137-18 MK585742 Northern Mindanao

BPHB103-16 MK585715 Taytay, Rizal





Desmalopex leucopterus BPHB205-19 MK622928 Palanan, Isabela





BPHB127-16 MK585796 Mt. Makiling, Laguna

Dyacopterus rickarti BPHB139-18 MK585794 Bukidnon

BPHB141-18 MK585790 Compostela Valley

BPHB140-18 MK585732 Compostela Valley

Eonycteris robusta BPHB199-19 MK622922 Palanan, Isabela

BPHB177-19 MK585740 Dona Remedios Trinidad, Bulacan











APPENDIX


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Eonycteris spelaea BPHB201-19 MK622924 Samal Island, Davao del Norte

BPHB200-19 MK622923 Samal Island, Davao del Norte




BPHB107-16 MK585741 Diliman, Quezon City

Haplonycteris fischeri BPHB119-16 MK585750 Palanan, Isabela









BPHB118-16 MK585747 Roxas, Oriental Mindoro





Harpyionycteris whiteheadi BPHB147-18 MK585744 Bukidnon



Macroglossus minimus BPHB207-19 MK622930 Palanan, Isabela





Megaerops wetmorei BPHB150-18 MK585770 Bukidnon



Nyctimene rabori BPHB152-18 MK585752 Sibuyan, Romblon

BPHB151-18 MK585748 Sibuyan, Romblon

Otopteropus cartilagonodus BPHB122-16 MK585758 Mt. Tapulao, Zambales

BPHB120-16 MK585729 Mt. Tapulao, Zambales





142

Ptenochirus jagori BPHB175-19 MK585812 Occidental Mindoro




BPHB104-16 MK585788 Manito, Albay










Ptenochirus minor BPHB154-18 MK585738 Bukidnon



Pteropus hypomelanus BPHB174-19 MK585778 Occidental Mindoro



Pteropus pumilus BPHB176-19 MK585724 Occidental Mindoro


BPHB165-19 MK585755 San Jose, Occidental Mindoro

Rousettus amplexicaudatus BPHB203-19 MK622926 Samal Island, Davao del Norte

BPHB202-19 MK622925 Samal Island, Davao del Norte







Styloctenium mindorensis BPHB158-18 MK585713 Occidental Mindoro

BPHB157-18 MK585749 Occidental Mindoro

BPHB156-18 MK585782 Occidental Mindoro


143

Species G e n b a n k Accession

BOLD Process ID

Macroglossus minimus HM540783 BM258-04

JQ365651 ABBSI327-11

HM540775 ABRVN444-06

HM540779 ABRVN440-06

HM540805 ABRSS028-06

HM540793 ABRSS043-06

HM540794 ABRSS044-06

HM540795 ABRSS045-06

HM540796 ABRSS074-06

HM540797 ABRSS075-06

HM540798 ABRSS076-06

JF459656 ABRSS079-06

HM540799 ABRSS080-06

JF459657 ABRSS081-06

HM540800 ABRSS082-06

HM540801 ABRSS083-06

HM540802 ABRSS084-06

HM540804 ABRSS086-06

HM540784 ABRSS087-06

HM540785 ABRSS088-06

HM540786 ABRSS112-06

HM540787 ABRSS113-06

HM540788 ABRSS114-06

HM540789 ABRSS115-06

HM540790 ABRSS116-06

HM540791 ABRSS117-06

HM540792 ABRSS118-06

HM540780 ABRVN439-06

HM540778 ABRVN441-06

HM540777 ABRVN442-06

HM540776 ABRVN443-06

HM540774 ABRVN445-06

HM540773 ABRVN446-06

HM540782 ABRVN447-06

HM540781 BM563-04

Macroglossus sobrinus HM540821 ABRVN452-06

HM540815 ABRVN459-06

HM540820 ABRVN453-06

HM540819 ABRVN454-06

HM540824 BM239-03

HM540828 ABBM251-05


BOLD Process ID

HM540809 ABBM291-05

GU684755 ABBSI128-09

GU684763 ABBSI136-09

HM540829 ABRSS335-06

HM540822 ABRVN451-06

HM540818 ABRVN455-06

HM540817 ABRVN456-06

HM540816 ABRVN457-06

HM540826 ABRVN458-06

HM540814 ABRVN460-06

HM540813 ABRVN461-06

HM540812 ABRVN462-06

HM540811 ABRVN463-06

HM540810 ABRVN464-06

HM540827 ABRVN465-06

HM540825 ABRVN572-06

HM540808 BM479-04

HM540823 BM565-04

HM540807 BM655-05

KY315495

KY315496

Melonycteris fardoulisi DQ487811 GBMA983-07

DQ487815 GBMA2211-09

DQ487809 GBMA985-07

DQ487814 GBMA2212-09

DQ487817 GBMA977-07

DQ487812 GBMA982-07

DQ487810 GBMA984-07

DQ487808 GBMA986-07

DQ487807 GBMA987-07

DQ487803 GBMA991-07

DQ487802 GBMA992-07

DQ487801 GBMA993-07

Melonycteris woodfordi DQ487794 GBMA1000-07

DQ487793 GBMA1001-07

DQ487792 GBMA1002-07

DQ487797 GBMA2215-09

DQ487796 GBMA2216-09

Rousettus aegyptiacus JF442679 ABCDC375-08

JF442630 ABCDC064-07

Table II. List of sequences downloaded from BOLD and Genbank.


144


BOLD Process ID

JF442632 ABCDC096-07

JF442633 ABCDC097-07

JF442634 ABCDC099-07

JF442636 ABCDC101-07

JF442637 ABCDC102-07

JF442638 ABCDC103-07

JF442639 ABCDC105-07

JF442640 ABCDC106-07

JF442641 ABCDC107-07

JF442642 ABCDC113-07

JF442644 ABCDC115-07

JF442645 ABCDC116-07

JF442646 ABCDC117-07

JF442647 ABCDC118-07

JF442648 ABCDC119-07

JF442649 ABCDC120-07

JF442650 ABCDC121-07

JF442651 ABCDC122-07

JF442653 ABCDC129-07

JF442654 ABCDC169-07

JF442655 ABCDC170-07

JF442656 ABCDC171-07

JF442657 ABCDC172-07

JF442658 ABCDC173-07

JF442659 ABCDC174-07

JF442662 ABCDC177-07

JF442663 ABCDC178-07

JF442664 ABCDC187-07

JF442665 ABCDC188-07

JF442666 ABCDC189-07

JF442667 ABCDC190-07

JF442668 ABCDC191-07

JF442669 ABCDC192-07

JF442670 ABCDC193-07

JF442671 ABCDC194-07

JF442678 ABCDC299-07

JF442673 ABCDC307-07

JF442675 ABCDC333-07

JF442676 ABCDC340-07

JF442677 ABCDC345-07

JF444434 ABRMM023-06

JF444435 ABRMM025-06

JF444436 ABRMM026-06


BOLD Process ID

JF444437 ABRMM027-06

JF444438 ABRMM028-06

JF444439 ABRMM029-06

JF444440 ABRMM030-06

JF444442 ABRMM032-06

JF444443 ABRMM060-07

JX282963 GBMA5663-13

JF728637 GBMA3961-12

ABBWP066-06

ABBWP211-07

ABBWP258-07

ABBWP354-07

Melonycteris melanops DQ487786 GBMA1008-07

DQ487791 GBMA1003-07

DQ487790 GBMA1004-07

DQ487789 GBMA1005-07

Eidolon helvum JF442371 ABCDC156-07

JF442372 ABCDC157-07

JF442373 ABCDC158-07

JF442374 ABCDC159-07

JF442375 ABCDC160-07

JF442376 ABCDC161-07

JF442377 ABCDC162-07

JF442378 ABCDC166-07

JF442379 ABCDC167-07

JF442380 ABCDC168-07

JF442383 ABCDC287-07

JF442384 ABCDC295-07

JF442385 ABCDC296-07

JF442386 ABCDC297-07

JF442387 ABCDC298-07

JF442381 ABCDC306-07

JF442382 ABCDC346-07

JX282936 GBMA5690-13

ABBWP308-07

ABBWP310-07

ABBWP322-07

ABBWP357-07

Pteropus hypomelanus JQ365652 ABBSI330-11


145


BOLD Process ID

Pteropus vampyrus HM541308 ABRVN411-06

HM541309 BM558-04

Cynopterus sphinx HM540231 ABCMA659-07

HM540229 ABCMA655-07

HM540230 ABCMA656-07

JQ599976 ABRCY108-06

JQ599941 ABRCY071-06

HM540240 ABRLA132-06

HM540219 ABCMA638-07

JQ599958 ABRCY090-06

HM540228 ABCMA654-07

HM540210 BM090-03

HM540216 BM167-03

HM540217 BM077-03

HM540215 ABBSI089-07

HM540214 ABBSI095-07

HM540213 ABBSI096-07

GU684748 ABBSI127-09

GU684776 ABBSI154-09

HM914954 ABBSI254-10

HM540234 ABCMA588-07

HM540220 ABCMA644-07

HM540221 ABCMA645-07

HM540222 ABCMA646-07

HM540223 ABCMA647-07

HM540224 ABCMA649-07

HM540225 ABCMA651-07

HM540226 ABCMA652-07

HM540227 ABCMA653-07

HM540232 ABCMA660-07

HM540233 ABCMA661-07

HM540235 ABCMA673-07

HM540236 ABCMA674-07

HM540237 ABCMA675-07

JQ599903 ABRCY029-06

JQ599904 ABRCY030-06

JQ599905 ABRCY031-06

JQ599906 ABRCY032-06

JQ599907 ABRCY033-06

JQ599908 ABRCY034-06

JQ599909 ABRCY035-06

JQ599910 ABRCY036-06


BOLD Process ID

JQ599911 ABRCY037-06

JQ599912 ABRCY038-06

JQ599913 ABRCY039-06

JQ599914 ABRCY040-06

JQ599915 ABRCY041-06

JQ599916 ABRCY042-06

JQ599917 ABRCY043-06

JQ599918 ABRCY044-06

JQ599919 ABRCY045-06

JQ599920 ABRCY047-06

JQ599921 ABRCY048-06

JQ599922 ABRCY049-06

JQ599923 ABRCY050-06

JQ599924 ABRCY051-06

JQ599925 ABRCY052-06

JQ599926 ABRCY055-06

JQ599927 ABRCY056-06

JQ599928 ABRCY057-06

JQ599929 ABRCY058-06

JQ599930 ABRCY059-06

JQ599931 ABRCY060-06

JQ599932 ABRCY061-06

JQ599933 ABRCY062-06

JQ599934 ABRCY063-06

JQ599935 ABRCY064-06

JQ599936 ABRCY065-06

JQ599937 ABRCY066-06

JQ599938 ABRCY067-06

JQ599939 ABRCY069-06

JQ599942 ABRCY072-06

JQ599943 ABRCY073-06

JQ599944 ABRCY074-06

JQ599945 ABRCY075-06

JQ599946 ABRCY076-06

JQ599947 ABRCY077-06

JQ599948 ABRCY078-06

JQ599949 ABRCY079-06

JQ599950 ABRCY080-06

JQ599952 ABRCY082-06

JQ599953 ABRCY083-06

JQ599954 ABRCY084-06

JQ599956 ABRCY086-06

JQ599957 ABRCY087-06


146


BOLD Process ID

JQ599959 ABRCY091-06

JQ599961 ABRCY093-06

JQ599964 ABRCY096-06

JQ599965 ABRCY097-06

JQ599967 ABRCY099-06

JQ599968 ABRCY100-06

JQ599969 ABRCY101-06

JQ599970 ABRCY102-06

JQ599979 ABRCY111-06

JQ599980 ABRCY112-06

JQ599981 ABRCY113-06

JQ599982 ABRCY114-06

JQ599983 ABRCY115-06

JQ599984 ABRCY116-06

JQ599985 ABRCY117-06

JQ599873 ABRCY136-06

JQ599874 ABRCY137-06

JQ599875 ABRCY139-06

HM540238 ABRLA082-06

HM540239 ABRLA083-06

HM540218 BM522-04

HM540209 BM594-04

JX282935 GBMA5691-13

HQ580344

KT291769

Pteropus giganteus KT291772

Pteropus lylei HM541306 ABRVN407-06

HM541305 ABRVN408-06

HM541304 ABRVN409-06

HM541302 ABRVN410-06

HM541307 ABRVN412-06

HM541303 BM557-04

KP975225

Rousettus amplexicaudatus HM541862 BM040-03

HM541861 BM186-03

HM541857 ABBM096-05

HM541858 ABBM107-05

HM541859 ABBM116-05

HM541863 ABBM117-05

HM541865 ABRLA133-06


BOLD Process ID

JF444109 ABRVN007-06

KY315501

Rousettus leschenaultii HM541873 ABCMA563-07

HM541874 ABCMA625-07

HM541870 ABCMA634-07

HM541871 ABCMA643-07

HM541872 ABCMA664-07

HM541875 ABCMA672-07

HM541876 ABCMA680-07

HM541877 ABCMA681-07

HM541878 ABCMA682-07

HM541879 ABCMA683-07

HM541880 ABCMA684-07

HM541881 ABCMA685-07

HM541882 ABCMA686-07

HM541883 ABCMA687-07

HM541884 ABCMA688-07

HM541885 ABCMA689-07

HM541886 ABRVN006-06

HM541867 ABRVN025-06

HM541868 ABRVN448-06

HM541869 BM562-04

KP975231

Eonycteris spelaea HM540258 ABRVN173-06

HM540261 ABRVN002-06

HM540254 ABRVN035-06

HM540257 ABBM095-05

HM540259 ABBM103-05

HM540251 ABBM316-05

JF443875 ABMUS064-06

HM540260 ABRVN001-06

HM540262 ABRVN003-06

HM540263 ABRVN004-06

HM540264 ABRVN005-06

HM540253 ABRVN036-06

HM540252 ABRVN037-06

HM540265 ABRVN392-06

HM540256 ABRVN449-06

HM540255 BM279-04

HM540249 BM451-04

HM540248 BM656-05


147


BOLD Process ID

KT291761

Scotonycteris zenkeri JF444229 ABRAF044-06

JF444230 ABRAF051-06

Lissonycteris angolensis JF442423 ABCDC198-07

JF442424 ABCDC204-07

JF442426 ABCDC214-07

JF442427 ABCDC215-07

JF442428 ABCDC219-07

JF442429 ABCDC220-07

JF442430 ABCDC221-07

JF442431 ABCDC222-07

JF442432 ABCDC223-07

JF442433 ABCDC224-07

JX282942 GBMA5684-13

JX282941 GBMA5685-13

JX282940 GBMA5686-13

JX282939 GBMA5687-13

KY385387

Myonycteris leptodon JX282958 GBMA5668-13

JX282957 GBMA5669-13

JX282956 GBMA5670-13

JX282955 GBMA5671-13

JX282954 GBMA5672-13

JX282953 GBMA5673-13

Myonycteris brachycephala JX282951 GBMA5675-13

JX282950 GBMA5676-13

Myonycteris torquata JX282962 GBMA5664-13

JX282961 GBMA5665-13

JX282960 GBMA5666-13

JX282959 GBMA5667-13

JF728636 GBMA3900-12

Myonycteris relicta JX282952 GBMA5674-13

Megaloglossus woermanni JF444181 ABRAF018-06

JF444182 ABRAF074-06

JX282945 GBMA5681-13

JX282944 GBMA5682-13


BOLD Process ID

JX282943 GBMA5683-13

Megaloglossus azagnyi JX282948 GBMA5678-13

JX282947 GBMA5679-13

JX282946 GBMA5680-13

Rousettus lanosus JX282965 GBMA5661-13

(Stenonycteris lanosus) JX282964 GBMA5662-13

Epomops franqueti JX282938 GBMA5688-13

JF728635 GBMA3962-12

Nanonycteris veldkampii JF444185 ABRAF096-06

JF444186 ABRAF097-06

JF444187 ABRAF098-06

JF444188 ABRAF099-06

JF444189 ABRAF100-06

JF444190 ABRAF111-06

Epomophorus wahlbergi JF442391 ABCDC271-07

JF442392 ABCDC273-07

JF442393 ABCDC277-07

JF442394 ABCDC280-07

JF442395 ABCDC347-07

JF442396 ABCDC348-07

JF442397 ABCDC349-07

Epomophorus labiatus JF442388 ABCDC275-07

JF442389 ABCDC290-07

JF442390 ABCDC292-07

ABBWP288-07

ABBWP299-07

ABBWP347-07

ABBWP367-07

ABBWP369-07

Micropteropus pusillus JX282949 GBMA5677-13

JF728610 GBMA3913-12

JF728608 GBMA3914-12

JF728606 GBMA3915-12

JF728604 GBMA3916-12

JF728602 GBMA3917-12

JF728600 GBMA3918-12


148


BOLD Process ID

JF728598 GBMA3919-12

JF728596 GBMA3920-12

JF728594 GBMA3921-12

JF728592 GBMA3922-12

JF728590 GBMA3923-12

JF728588 GBMA3924-12

JF728586 GBMA3925-12

JF728584 GBMA3926-12

JF728582 GBMA3927-12

JF728580 GBMA3928-12

JF728578 GBMA3929-12

JF728576 GBMA3930-12

JF728574 GBMA3931-12

JF728572 GBMA3932-12

JF728570 GBMA3933-12

JF728568 GBMA3934-12

JF728566 GBMA3935-12

JF728564 GBMA3936-12

JF728562 GBMA3937-12

JF728560 GBMA3938-12

JF728558 GBMA3939-12

JF728556 GBMA3940-12

JF728554 GBMA3941-12

JF728552 GBMA3942-12

JF728550 GBMA3943-12

JF728548 GBMA3944-12

JF728546 GBMA3945-12

JF728544 GBMA3946-12

JF728542 GBMA3947-12

JF728540 GBMA3948-12

JF728538 GBMA3949-12

JF728536 GBMA3950-12

JF728534 GBMA3951-12

JF728532 GBMA3952-12

JF728530 GBMA3953-12

JF728528 GBMA3954-12

JF728526 GBMA3955-12

JF728524 GBMA3956-12

JF728522 GBMA3957-12

JF728520 GBMA3958-12

JF728518 GBMA3959-12

JF728516 GBMA3960-12

JF728611 GBMA3974-12


BOLD Process ID

JF728609 GBMA3975-12

JF728607 GBMA3976-12

JF728605 GBMA3977-12

JF728603 GBMA3978-12

JF728601 GBMA3979-12

JF728599 GBMA3980-12

JF728597 GBMA3981-12

JF728595 GBMA3982-12

JF728593 GBMA3983-12

JF728591 GBMA3984-12

JF728589 GBMA3985-12

JF728587 GBMA3986-12

JF728585 GBMA3987-12

JF728583 GBMA3988-12

JF728581 GBMA3989-12

JF728579 GBMA3990-12

JF728577 GBMA3991-12

JF728575 GBMA3992-12

JF728573 GBMA3993-12

JF728571 GBMA3994-12

JF728569 GBMA3995-12

JF728567 GBMA3996-12

JF728565 GBMA3997-12

JF728563 GBMA3998-12

JF728561 GBMA3999-12

JF728559 GBMA4000-12

JF728557 GBMA4001-12

JF728555 GBMA4002-12

JF728553 GBMA4003-12

JF728551 GBMA4004-12

JF728549 GBMA4005-12

JF728547 GBMA4006-12

JF728545 GBMA4007-12

JF728543 GBMA4008-12

JF728541 GBMA4009-12

JF728539 GBMA4010-12

JF728537 GBMA4011-12

JF728535 GBMA4012-12

JF728533 GBMA4013-12

JF728531 GBMA4014-12

JF728529 GBMA4015-12

JF728527 GBMA4016-12

JF728525 GBMA4017-12


149


BOLD Process ID

JF728523 GBMA4018-12

JF728521 GBMA4019-12

JF728519 GBMA4020-12

JF728517 GBMA4021-12

JF728515 GBMA4022-12

Epomophorus gambianus JX282937 GBMA5689-13

JF728634 GBMA3901-12

JF728632 GBMA3902-12

JF728630 GBMA3903-12

JF728628 GBMA3904-12

JF728626 GBMA3905-12

JF728624 GBMA3906-12

JF728622 GBMA3907-12

JF728620 GBMA3908-12

JF728618 GBMA3909-12

JF728616 GBMA3910-12

JF728614 GBMA3911-12

JF728612 GBMA3912-12

JF728633 GBMA3963-12

JF728631 GBMA3964-12

JF728629 GBMA3965-12

JF728627 GBMA3966-12

JF728625 GBMA3967-12

JF728623 GBMA3968-12

JF728621 GBMA3969-12

JF728619 GBMA3970-12

JF728617 GBMA3971-12

JF728615 GBMA3972-12

JF728613 GBMA3973-12

Megaerops niphanae HM540869 BM174-03

HM540867 ABRVN192-06

HM540842 BM021-03

HM540852 BM067-03

HM540849 BM185-03

HM540851 BM187-03

HM540846 BM200-03

HM540850 BM224-03

HM540843 ABBM112-05

HM540848 ABBM137-05

HM540844 ABBM187-05

HM540845 ABBM225-05


BOLD Process ID

HM540874 ABRLA061-06

HM540875 ABRLA131-06

HM540876 ABRLA152-06

HM540877 ABRLA153-06

HM540866 ABRVN205-06

HM540865 ABRVN213-06

HM540864 ABRVN214-06

HM540870 ABRVN215-06

HM540863 ABRVN216-06

HM540862 ABRVN219-06

HM540861 ABRVN220-06

HM540860 ABRVN221-06

HM540859 ABRVN222-06

HM540858 ABRVN231-06

HM540857 ABRVN232-06

HM540856 ABRVN233-06

HM540855 ABRVN241-06

HM540854 ABRVN242-06

HM540853 ABRVN246-06

HM540871 ABRVN325-06

HM540847 ABRVN404-06

HM540872 ABRVN497-06

HM540873 ABRVN498-06

HM540868 BM529-04

HQ580345

HQ580346

Megaerops wetmorei HM540878 BM480-04

Megaerops kusnotoi HM540840 BM278-03

Megaerops ecaudatus JF443968 ABRSS360-06

HM540839 BM428-04

Cynopterus titthaecheilus HM540241 BM267-03

JQ599876 ABRCY001-06

Cynopterus brachyotis HM540199 BM260-03

HM540198 BM270-03

JN312461 ABRCY002-06

HM540201 BM183-03

HM540196 ABBSI039-04

JQ599877 ABRCY003-06


150


BOLD Process ID

JQ599879 ABRCY005-06

JQ599880 ABRCY006-06

JQ599940 ABRCY070-06

JQ599951 ABRCY081-06

JQ599955 ABRCY085-06

JQ599960 ABRCY092-06

JQ599962 ABRCY094-06

JQ599963 ABRCY095-06

JQ599966 ABRCY098-06

JQ599971 ABRCY103-06

JQ599972 ABRCY104-06

JQ599973 ABRCY105-06

JQ599974 ABRCY106-06

JQ599975 ABRCY107-06

JQ599977 ABRCY109-06

JQ599978 ABRCY110-06

HM540200 BM564-04

HM540195 BM614-04

HM540203 BM433-04

HM540202 BM273-03

Cynopterus JLE JQ599878 ABRCY004-06

JQ599881 ABRCY007-06

JQ599882 ABRCY008-06

JQ599883 ABRCY009-06

JQ599884 ABRCY010-06

JQ599885 ABRCY011-06

JQ599886 ABRCY012-06

JQ599887 ABRCY013-06

JQ599888 ABRCY014-06

JQ599889 ABRCY015-06

JQ599890 ABRCY016-06

JQ599891 ABRCY017-06

JQ599892 ABRCY018-06

JQ599893 ABRCY019-06

JQ599894 ABRCY020-06

JQ599895 ABRCY021-06

JQ599896 ABRCY022-06

JQ599897 ABRCY023-06

JQ599898 ABRCY024-06

JQ599899 ABRCY025-06

JQ599900 ABRCY026-06

JQ599901 ABRCY027-06


BOLD Process ID

JQ599902 ABRCY028-06

JQ599851 ABRCY118-06

JQ599852 ABRCY120-06

JQ599853 ABRCY121-06

JQ599854 ABRCY122-06

JQ599855 ABRCY124-06

JQ599856 ABRCY125-06

JQ599859 ABRCY128-06

JQ599860 ABRCY129-06

JQ599861 ABRCY131-06

JQ599862 ABRCY132-06

Cynopterus horsfieldii HM540206 BM445-04

JQ599865 ABRCY135-06

HM540207 BM543-04

Balionycteris maculata HM540174 BM437-04

HM540183 BM271-03

JF443874 ABRSS077-06

HM540189 ABRSS149-06

HM540184 ABRSS157-06

HM540185 ABRSS158-06

HM540186 ABRSS184-06

HM540187 ABRSS185-06

HM540188 ABRSS207-06

HM540181 ABRSS309-06

HM540182 ABRSS315-06

HM540176 ABRSS327-06

HM540177 ABRSS328-06

HM540178 ABRSS329-06

HM540179 ABRSS355-06

HM540180 ABRSS382-06

KY315483

KY315485

KY315486

KY315488

Chironax melanocephalus HM540191 BM266-03

Aethalops alecto JF459622 ABRSS147-06

HM540124 ABRSS148-06

HM540110 ABRSS159-06

HM540111 ABRSS182-06


151


BOLD Process ID

HM540112 ABRSS183-06

HM540113 ABRSS195-06

HM540114 ABRSS196-06

HM540115 ABRSS197-06

HM540116 ABRSS208-06

HM540117 ABRSS247-06

HM540118 ABRSS285-06

HM540119 ABRSS286-06

HM540120 ABRSS287-06

HM540121 ABRSS295-06

HM540122 ABRSS296-06

HM540123 ABRSS297-06

HM540109 BM282-04

Sphaerias blanfordi HM541952 ABCMA657-07

HM541954 ABCMA663-07

HM541942 BM370-04

HM541962 ABBSI088-07

HM541955 ABCMA562-07

HM541956 ABCMA581-07

HM541957 ABCMA582-07

HM541958 ABCMA583-07

HM541959 ABCMA584-07

HM541960 ABCMA585-07

HM541943 ABCMA589-07

HM541944 ABCMA590-07

HM541945 ABCMA591-07

HM541946 ABCMA592-07

HM541947 ABCMA610-07

HM541950 ABCMA636-07

HM541951 ABCMA637-07

HM541953 ABCMA662-07

HM541948 ABCMA676-07

HM541949 ABCMA677-07

HM541961 ABRVN547-06

Penthetor lucasi HM541198 ABRSS224-06

HM541199 ABRSS225-06

HM541182 ABRSS209-06

HM541186 ABRSS210-06

HM541187 ABRSS211-06

HM541188 ABRSS212-06

HM541189 ABRSS213-06


BOLD Process ID

HM541190 ABRSS214-06

HM541191 ABRSS215-06

HM541183 ABRSS216-06

HM541184 ABRSS217-06

HM541192 ABRSS218-06

HM541193 ABRSS219-06

HM541194 ABRSS220-06

HM541195 ABRSS221-06

HM541196 ABRSS222-06

HM541197 ABRSS223-06

HM541200 ABRSS249-06

HM541185 ABRSS250-06

HM541201 ABRSS251-06

HM541202 ABRSS270-06

HM541181 BM492-04


152

dna barcodes reveal high genetic diversity in philippine fruit bats · 2019. 10. 9. · keywords:...

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