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Goh et al.: Genetic diversity of house-farm swiftlets

Genetic diversity among white-nest swiftlets of the genus Aerodramus (Aves: Apodidae: Collocaliini) of house-farms in Malaysia

W.L. Goh1*, W.S. Siew1, S.E.W. Davies 2, S. Ball2, G. Khoo1, C.K. Lim3, M. A. Rahman4, Earl of Cranbrook5

Abstract. The swiftlets (Aves, Apodidae, Collocaliini) have been known as producers of edible nests for four centuries. Among the genus Aerodramus Oberholser 1912 ecological evidence and museum specimens support the existence of two wild species making ‘white’ edible nests: grey-rumped swiftlet Aerodramus inexpectatus (Hume, 1873), a species occurring on islands, rocky stacks and maritime cliffs from the Andaman Islands to the north-east coast of Borneo, and brown-rumped swiftlet A. fuciphagus (Thunberg, 1812), occurring at inland sites only in Borneo, but at inland and island localities in Sumatra, Java, and Nusa Tenggara Barat, Indonesia. House-farm swiftlets, which make similar white nests, were first recorded as spontaneous occupiers of buildings in Java, Indonesia, in the late 19th century, presumably from A. fuciphagus stock. In Peninsular Malaysia and Singapore, the first observations of nesting in buildings were made later, from 1931 to 1947. Subsequent human intervention has greatly expanded the numbers and range of house-farms, first in Java and elsewhere in Indonesia by fostering eggs in the nests of Linchi Swiftlets Collocalia linchi, and latterly by the use of recorded vocalisations to attract birds into purpose-made buildings. During the 20th and early 21st centuries, house-farm swiftlets and ‘house-farming’ have largely replaced wild colonies as sources of white nests. Previous genetic evidence based on mitochondrial DNA (mtDNA) has supported species level separation of the two wild white-nest species but more recent genetic studies have questioned this conclusion. The present study has focused on mitochondrial genetics with new samples of swiftlets from house-farms in Peninsular and Bornean Malaysia, and wild grey-rumped swiftlets Aerodramus inexpectatus on the islands of Mantanani Besar, Sabah, and Seringgis, Terengganu. GenBank data were used to extend comparisons to include house-farm swiftlet mtDNA from southern Thailand and Vietnam. Re-analysis of the three previous studies of genetic diversity in house-farm swiftlets coupled with the new supplementary data of mitochondrial cytochrome-b shows that the multiple maternal lineages observed within the house-farm swiftlets of Malaysia can also be detected more widely across the Southeast Asian region. In conclusion, we argue that house-farm swiftlets exhibit behavioural characters that could be considered evidence of domestication. We hope to see further studies using fuller genome sequencing to give improved insights into the phylogenetics of the progressive domestication of house-farm white-nest swiftlets.

Key words. domestication, house-farming, Malaysia, Indonesia, mitochondrial DNA markers, nuclear DNA markers, white-nest swiftlets

RAFFLES BULLETIN OF ZOOLOGY 66: 350–360Date of publication: 22 June 2018http://zoobank.org/urn:lsid:zoobank.org:pub:07C8CB8F-064A-4D03-BCEC-8211B135F461

© National University of SingaporeISSN 2345-7600 (electronic) | ISSN 0217-2445 (print)

1Department of Biological Science, Faculty of Science, Universiti Tunku Abdul Rahman, Jalan Universiti, Bandar Barat, 31900 Kampar, Perak, Malaysia; Email: [email protected] (*corresponding author)2Micropathology, Ltd, University of Warwick Science Park, Venture Centre, Sir William Lyons Road, Coventry CV4 7EZ, United Kingdom3157, Lorong 4A, Off Jalan Stampin Timur, 93300 Kuching, Sarawak, Malaysia4Faculty of Natural Science and Sustainability, University College Sabah Foundation, Jalan Sanzac, 88100 Sembulan, Kota Kinabalu, Sabah5International Collaborative Partner, Universiti Tunku Abdul Rahman Global Research Network, and Honorary Research Fellow, Micropathology Ltd.

INTRODUCTION

The taxonomy of white-nest swiftlets. The swiftlets form a natural group of birds (Apodidae, Collocaliini) distributed at tropical or sub-tropical latitudes across the Indo-Pacific region from the Seychelles to Hawai’i, north

to the eastern Himalayas in continental Asia, and south to northern Australia (Chantler, 2005). For four centuries, swiftlets have been noted in Western ornithology for their edible nests (Ray, 1678: 215). In a review of the group of swiftlets that includes the main producers of edible nests, now placed in the genus Aerodramus Oberholser, 1912, the great evolutionary taxonomist Ernst Mayr (1937: 1–2) wrote: “Every author who has worked with these small swiftlets of the Indo-Australian region will contend that their classification presents the most difficult problem in the taxonomy of birds. The members of this genus live in large or small colonies, frequently in inaccessible caves, and every population is slightly different from the next one... To make matters worse, most of the species are of practically the same dull sooty gray colouration with almost the same development of the structural characters (such as bill, feet, wing formula, etc)”. A notable exception to the lack of differentiation in the plumage is found between sympatric populations of Aerodramus swiftlets in northern Borneo. Here, by his collections (now in the Lee Kong Chian Natural

Taxonomy & Systematics

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History Museum, Singapore), Chasen (1931) demonstrated that the swiftlets making ‘white’ edible nests on islands and rocky marine stacks around the coast, including Berhala islet in Sandakan harbour, were distinguished by a well-defined white or pale grey bar across the rump, contrasting with dark back and tail (Plate 1), while those swiftlets making similar ‘white’ nests in Gomantong caves, “only a few miles away and within sight of Berhala”, and in other inland caves at Baturong, Madai, and Tapadong (Plate 2) had a dark rump, uniformly coloured with back and tail. Chasen interpreted the geographical proximity of the two forms as evidence of separation at species level. Accordingly, using the accepted systematic and English nomenclature of his time, Chasen (1935: 114–115) recognised grey-rumped swiftlets, Collocalia francica (Gmelin, 1789), represented in coastal islands of Borneo by C. f. germani Oustalet, 1876 and C. f. perplexa Riley, 1927 and in the Thai-Malay Peninsula to Java and Nusa Tenggara Barat, Indonesia, by a cline of darkening rump colour consisting of named subspecies C. f. germani, C. f. amechana Oberholser, 1912, C. f. javensis Stresemann, 1931 and C. f. bartelsi Stresemann, 1927; and brown-rumped swiftlets Collocalia vestita (Lesson, 1843), with C. v. vestita occurring in Sumatra and its satellite islands and C. v. maratua Riley, 1927 in mainland Borneo and the Maratua islands.

There have subsequently been changes in the systematic nomenclature of these swiftlets but, for three decades, the distinctness of two white-nest species, grey-rumped swiftlet and brown-rumped swiftlet, remained consensus in Malaysian scientific and popular literature, exemplified by Delacour (1947), Gibson-Hill (1949), Glenister (1951, reprinted 1971) and Smythies (1957, 1960). An alternative interpretation of the evidence, as a ‘circle of races’ (Rassenkreis), was proposed by Medway (1966), by which grey-rumped and brown-rumped swiftlets were combined in a single species for which the prior name was Aerodramus fuciphagus (Thunberg, 1812). For a period, this interpretation was generally accepted in ornithological literature (Chantler, 2005), until Cranbrook et al. (2013) re-examined historical museum specimens on which the taxonomic decisions of Chasen (1935) and Gibson-Hill (1949) had been based. In the historic museum skins collected (by shooting) in southern Peninsular Malaysia there is a discernible break in rump colour and not an intergraded cline. Where the two species meet but remain ecologically separate, respectively on islands and the mainland of Borneo, there is a clear morphological separation between grey-rumped swiftlets, for which the prior species name is A. inexpectatus (Hume, 1873) and brown-rumped A. fuciphagus. These observations have confirmed the identity of grey-rumped swiftlets Aerodramus inexpectatus germani and A. i. perplexus on Bornean islands and brown-rumped swiftlets A. fuciphagus vestitus in caves of inland Borneo.

House-farmed swiftlets: progress of a new domestication. The only known case of translocation of adult swiftlets followed by the establishment of a self-sustaining population, albeit small, is the trans-oceanic introduction of the Guam swiftlet Aerodramus bartschi (Mearns, 1909) to Oahu,

Plate 1. Grey-rumped Swiftlet, Aerodramus inexpectatus germani from Gua Gabnor (Governor’s cave), Mantanani Besar Island, Sabah, Malaysia.

Plate 2. A skin of Brown-rumped Swiftlet, Aerodramus fuciphagus vestitus, collected in Gomantong Cave, Sabah, by F. N. Chasen, now in Lee Kong Chian Museum, reg. no, 3-9545.

Plate 3. Eggs of house-farm swiftlets collected for transfer to the nests of Linchi Swiftlet Collocalia linchi in a partially converted house-farm at Sajira, West Java, Indonesia, by courtesy of Dr Boedi Mranata.

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Hawai’i (Chantler, 2005). Among the house-farm white-nest swiftlets, other human directed processes have operated. Dated observations of the occupation of buildings show that spontaneous dispersal of birds has been a significant factor. Additionally, people have responded to, and channelled behavioural change among white-nest swiftlets in an interactive process involving humans and birds. Visible consequences of these developments have been monitored since 1957 by EoC, whose archive of published and unpublished reports, field notes and other observations, film, photographs and digital images has been deposited at the Lee Kong Chian Natural History Museum, Singapore. Reference to these sources is cited below as Archive.

The first instances of white-nest swiftlets spontaneously occupying buildings occurred in Java, Indonesia, in the late 19th century (Lim & Cranbrook, 2014), i.e. the region occupied by typical Aerodramus f. fuciphagus. In confirmation of this date, in 1960, at a large country house near Jakarta, Medway (1961a) was told that the birds nesting in outbuildings had been present for about 60 years. In 1960, established colonies were noted in a variety of buildings, including a department store, Toko Jap, in Jakarta, dwellings and shophouses in Bogor and other towns, and the outbuildings of rural properties. While some proprietors took no action, others reduced the entrances used by the birds, both to darken the nesting area and to protect against intruders, and also modified the interior to increase the ceiling area for attachment of nests (Medway, 1961a). In Singapore, Chasen (1939) reported earlier observations of “large numbers seeking the shady shelter of large stone-walled rooms, or vaults in buildings, in the late afternoon for roosting purposes: they were easily caught with a large butterfly-net”, adding in a footnote: “There is now a breeding colony of these birds in a much-frequented large building in Singapore”. Chasen himself (1939) considered that these birds were indistinguishable from white-nest swiftlets of Java. Skins from his collections of 1931 are preserved in the Lee Kong Chian Natural History Museum (Archive). In Peninsular Malaysia, first observations of established colonies in buildings were noted in 1947 in Penang, and in Kuala Lumpur in 1948 (Gibson-Hill, 1949). Anecdotal reports point to spontaneous occupation of buildings during the 1950–60s in Taiping, Perak, and Kuala Terengganu (Archive).

In Java, in the 1970s it was discovered that, if eggs of white-nest swiftlets were transferred to active nests of Linchi swiftlet Collocalia linchi Horsfield & Moore, 1854, the recipient pair would incubate and rear the fostered young. In response, a market for eggs from white-nest colonies arose, with eggs being transported in styrofoam sheets and sold at an average of Rp 3000 (=US 0.35 cents) apiece (Archive, Plate 3). Since outhouses or barns occupied by Linchi swiftlets were widespread in urban and rural locations, through the 1980–90s this practice greatly expanded the range of house-farm white-nest swiftlets within the island of Java. Eggs from Java were also transported to other parts of Indonesia, with successful instances of conversion in buildings occupied by other Collocalia species or subspecies being noted in East Kalimantan, Collocalia affinis cyanoptila Oberholser, 1906

(Lim & Cranbrook, 2014) and Lombok, Nusa Tenggara Barat, Collocalia linchi dedii Somadikarta, 1986 (Archive).

A more significant development followed in the 1980s, when it was found that recorded vocalisations were effective in attracting white-nest swiftlets into buildings. At the same time, distinctive architectural styles emerged with internal structures including rooms, stairs and other features intended to meet the combined requirements of human managers and breeding swiftlets. Based on their experience in Java, local authors described these designs, with recommended management procedures, in instructive manuals of this time (Archive: Fatich Marzuki, 1994; Wiboyo, 1995; Nugroho et al., 1996). Acting together, these practices led to a steady increase in the regional population of white-nest swiftlets that were instinctively entrained to seek buildings as nesting sites.

During the 1990s, the use of recorded vocalisations emitted from microphones strategically placed in architecturally designed buildings became the predominant practice. Simultaneously, encouraged by widespread investment in new ‘swiftlet houses’, the increasing regional population expanded by natural dispersion through Sumatra, southern Thailand and Peninsular Malaysia (Archive). Northward expansion from Thailand into interior Vietnam may have been earlier: Nguyen Quang & Voisin (2007) provided evidence that white-nest swiftlets had spontaneously colonised buildings in seven Vietnamese towns starting about 1970.

A dramatic extension of range across the South China Sea occurred in the mid-1990s, when new arrivals in Miri, northeastern Sarawak, plastered their nests under porches and around window-frames, as if begging to be let in (Cranbrook, pers. obs.). Westward along the Sarawak coast, in Bintulu in 1997, LCK and EoC saw some 18 nests built around the eaves of the Malaysian Airlines office, apparently unnoticed by inhabitants of the town. By the following year, observant owners of nearby top-floor apartments had opened their windows and by 2005 there were several thriving colonies in the town centre (Lim & Cranbrook, pers. obs).

As a consequence of these developments, throughout South-east Asia during the 20th and early 21st centuries, the harvests from house-farm swiftlets and ‘house-farming’ have effectively replaced wild colonies as sources of white nests in the market (Thorburn, 2014, 2015). In urban areas of Malaysia, the impact of house-farming has created social pressures (Connolly, 2016a, b; 2017a, b). For conservation of wild populations, the outcome has not been favourable. In northern Borneo, natural populations of grey-rumped and brown-rumped swiftlets are now seriously depleted by uncontrolled harvesting at unsustainable levels (Mallinson et al., 2015). Grey-rumped swiftlet colonies in rocky islets or sea caves of the small islands of Peninsular Malaysia are also reduced to very low numbers (Goh, Siew & Cranbrook, pers. obs. 2016).

Molecular evidence and the genetics of house-farm swiftlets. Molecular evidence based on mitochondrial genes initially supported the recognition of two wild white-nest

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species. Lee et al. (1996) showed separation equivalent to the genetic distance between morphological species, distinguishing grey-rumped swiftlets of Balambangan Island, Sabah, from brown-rumped swiftlets taken at Gomantong caves, Sabah. Price et al. (2004) and Thomassen et al. (2005, p. 161, Fig. 1) amplified these results, again showing as great or greater genetic distance between grey-rumped swiftlets and brown-rumped swiftlets as between many clades recognised on behavioural and morphological grounds as distinct species.

In a fuller investigation of the phylogenetic history of genus Aerodramus, Rheindt et al. (2014) obtained new sequences of a 406 bp fragment of mtDNA cytochrome-b from four individuals of three species. For a further 47 individuals of some 15 species (and a greater number of taxa at subspecific level) these authors drew on GenBank sequences. Two sequences, EU594263 and EU594264, identified as A. fuciphagus amechanus, from Selangor, ‘specimen or blood’; collectors A.R. Mustafa and W.L. Goh (Rheindt et al., 2014, Table 2) show an anomalous affinity with Aerodramus hirundinaceus. The status of the name amechanus was discussed by Cranbrook et al. (2013), showing that it is not applicable to swiftlets from Peninsular Malaysia. Genbank depositors GWL and MAR take this opportunity to clarify that these samples were eggs, taken from house-farm colonies, which we do not now identify as A. f. amechanus. Neither sample was used for the sequences in Cranbrook et al. (2013).

Identity of house-farm swiftlets. Past nomenclature in the literature has assumed that white-nest swiftlets occupying buildings were drawn from local wild populations. Thus, Chasen (1939; 129) identified the birds nesting in a building in Singapore as southern grey-rumped swiftlet, under the systematic name Collocalia francica amechana. Gibson-Hill (1949: 109–110) named the Penang birds northern grey-rumped swiftlet, Collocalia francica germani; and those in the Federal Survey Office, Kuala Lumpur, and others in an office building in Robinson Road, Singapore, as southern grey-rumped swiftlet, C. francica amechana. Following recognition that Hirundo fuciphaga Thunberg, 1812 was the prior species name for the white-nest swiftlet of Java (Medway, 1961b), Medway & Wells (1976) named birds nesting in the Town Hall, Kuala Lumpur as Collocalia fuciphaga. Brooke (1972) separated the grey-brown echo-locating swiftlets as genus Aerodramus and this nomenclature was followed by Langham (1980), who named the Penang colony as Aerodramus fuciphagus. Only Nguyen Quang & Voisin (2007: 54−55) were unable to identify ‘Vietnamese house swiftlets’ (their name) as any wild species or subspecies in the region.

In Sarawak and Sabah, house-farm swiftlets show variable plumage characters, often including a grey rump, but are separable from both brown-rumped swiftlet, now A. fuciphagus vestitus, and grey-rumped swiftlet, A. inexpectatus germani of island colonies (Cranbrook et al., 2013). In

Fig. 1. One of the six equally parsimonious trees rooted with Collocalia esculenta. Bootstrap values shown above the nodes. Posterior probabilities from Bayesian Inference shown below the nodes.

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Peninsular Malaysia there are no natural inland populations of a white-nest swiftlet. The only wild colonies are grey-rumped swiftlets nesting on islands off both coasts (Wells, 1999). Despite thousands of house-farms now found throughout Peninsular Malaysia, there are no records of white-nest swiftlets reverting to cave nesting sites in limestone-rich areas such as the neighbourhood of Ipoh, Perak, or at Batu Caves, Selangor (authors, pers. obs.).

Of the three previous genetic studies of house-farm swiftlets, Thi Loan et al. (2015) sampled birds of Vietnam and concluded that the genetic difference between house-farm swiftlets and the local wild species of white-nest swiftlets (Aerodramus inexpectatus germani) justified taxonomic separation. Along the coast of southern Thailand, Aowphol et al. (2008) found considerable gene flow among house-farm colonies and concluded that all were part of a single panmictic population. Further south, across a broad band from North Sumatra, both coasts of Peninsular Malaysia and Sarawak, in samples of embryos (in eggs) and tissue of 49 house-farm individuals, Cranbrook et al. (2013) found evidence of substantial gene flow among house-farm swiftlets, but also the existence of two clades likely to reflect a difference in origin. Clade 1 included house-farm swiftlets from the entire geographical range sampled, broadly between 2–4°N and 99–114°E, but it excluded haplotypes of wild birds including brown-rumped swiftlets A. fuciphagus vestitus of Middle Baram, Sarawak, and two GenBank sequences attributable to grey-rumped swiftlets A. inexpectatus germani from Sabah (Price et al., 2004). Clade 2 included nine house-farm swiftlets from the west and east coasts of Peninsular Malaysia and Sibu, Sarawak, i.e. approximately 2–4°N and 100–114°E, along with specimen DHC04, collected on Balambangan Island, Sabah, 7.267°N 116.917°E, identified as ‘Germain’s Swiftlet’, i.e. A. i. germani by Price et al. (2004).

The present study. In the following pages, we extend preliminary investigations into the phylogenetics of the morphologically variable house-farm swiftlets of Malaysia (Cranbrook et al., 2013) by including three wild white-nest swiftlet subspecies in Malaysia. This contribution also consolidates DNA data sourced from Thailand (Aowphol et al., 2008) and Vietnam (Thi Loan et al., 2015) with new, extended partial mitochondrial sequences.

MATERIALS AND METHODS

Sample collection. All birds handled were given a unique collection number. Single primary feathers (remiges) were plucked symmetrically from each wing (in most cases the 3rd or 4th primary, on two occasions the 6th, numbered centripetally), the feather bases cut off and preserved in 70% ethanol, from living swiftlets caught in house-farms. In Peninsular Malaysia, house-farms were sampled at Bachok and Tanah Merah, Kelantan; Kemaman, Terengganu; Mentakab and Bentong, Pahang; and Slim River and Sitiawan, Perak, and a natural colony of grey-rumped swiftlets Aerodramus inexpectatus in a sea cave on Pulau Seringgis, Perhentian Islands. In Sabah, Malaysia, house-farms were sampled at Tanjung Aru and Penampang, near

Kota Kinabalu, and Jalan Tander and Jalan Selaping, Kota Marudu, and a wild colony of A. inexpectatus germani in Gua Gabnor, Pulau Mantanani Besar. Nest specimens of A. f. vestitus were obtained from Middle Baram, Sarawak. The specimens and locations of the white-nest swiftlets, as well as those for black-nest swiftlets, A. maximus, and mossy-nest swiftlets, A. salanganus, are listed in Tables 1 and 2.

Molecular methods and data analyses. Total DNA was extracted from the samples using a HiYield Plus™ Genomic DNA Mini Kit (Blood/Tissue/Cultured Cells) following the manufacturer’s protocol. Partial mitochondrial cytochrome-b (cyt-b) and NADH dehydrogenase 2 (ND2) regions were amplified following the protocol described in Thomassen et al. (2005) and Cranbrook et al. (2013). Amplicons were commercially sequenced by 1stBase Laboratories Sdn. Bhd. or MyTACG Sdn. Bhd. Multiple sequence alignment was performed using ClustalX (Thompson et al., 1997) and Bioedit (Hall, 1999). A partition homogeneity (PH) test was performed in PAUP4.0 b10 (Swofford, 2002) before the cyt-b and ND2 data were combined. Haplotypes were identified using DnaSP (Librado & Rozas, 2009). All DNA sequences obtained in this study were deposited in GenBank (accession nos. MG322690 – MG322745). Additional DNA sequence data of four specimens of A. fuciphagus and A. maximus published by Price et al. (2004) were retrieved from GenBank (AY294429, AY294491, AY294428, AY294490, AY294449, AY294511, AY294445, AY294509) and included in the analysis for comparison. Collocalia esculenta (Price et al., 2004) was used as the outgroup.

For phylogenetic analyses, a strict consensus Maximum Parsimony (MP) tree was reconstructed using PAUP4.0 b10 (Swofford, 2002). The heuristic search was set at 100 random sequence additions and the branch swapping algorithm used was Tree Bisection and Reconnection (TBR). Bootstrapping was performed at 1,000 replications. Bootstrap values > 70% were considered strong support.

The best-fit model (GTR+G) for Bayesian Inference (BI) was chosen by MrModeltest2.2 (Nylander, 2004). BI analyses were run in MrBayes3.1 (Huelsenback & Ronquist, 2001) using two runs of four chains each, and run for 10,000,000 generations with trees sampled every 100 generations. The first 2,500 trees were discarded as burn-in. Posterior probabilities (PP) > 0.90 were considered strong support in this study. For the house-farm swiftlets and the wild colony of Middle Baram, population pairwise FST analysis was performed in Arlequin 3.5 (Excoffier & Lischer, 2010). “Population” was defined based on geographical zonation for the individuals in Clade 1 (Fig. 1) whereas all individuals in Clade 2 were set as a separate “population” (Table 1).

RESULTS AND DISCUSSION

Aligned DNA sequences formed data matrices of 817 bp for cyt-b and 396 bp for ND2. Data combination was supported by the partition homogeneity (PH) test. Among the 68 house-farm individuals, 17 haplotypes were recognised (Table 1). Identical sequences within the wild swiftlet species were

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also synchronised into haplotypes and listed in Table 2. Phylogenetic trees show that all house-farm swiftlets form a moderately supported cluster with brown-rumped swiftlet A. f. vestitus (BS 78%; PP < 0.90, not shown in the tree). The Sabah grey-rumped swiftlet A. i. germani clade is outside this cluster, while A. salanganus is isolated from all white-nest swiftlet lineages (Fig. 1). The grey-rumped swiftlets collected from Terengganu sea caves (Hap26) appear to be closely related to A. i. germani; a formal description for nomenclatural purposes requires additional samples. In other words, on the basis of this new evidence, despite dissimilarity in plumage characters, all Malaysian house-farm swiftlets are genetically closer to the Borneo representative of the brown-rumped swiftlet A. fuciphagus vestitus than to either local representatives of grey-rumped swiftlets A. inexpectatus.

Within house-farmed swiftlets, pairwise FST comparison between population pairs suggested significant genetic distinction between the house-farm individuals in Clade 2 and those of Clade 1 (Table 3). Clade 1, representing the majority of house-farm swiftlets across Peninsular Malaysia and the Borneo States of Malaysia, shows the signature of substantial mitochondrial gene flow among “populations”. Clade 2, on the other hand, is less abundant, less widespread and predominantly found in Mentakab and Bentong, Pahang, Peninular Malaysia. The pairwise FST comparison corroborates the phylogenetic data that both clades 1 and 2 are genetically separable from A. f. vestitus collected in the Middle Baram, Sarawak.

Does the two-clade pattern also occur in Thailand and Vietnam? Aowphol et al. (2008) concluded that the house-farm swiftlet colonies in Thailand, regardless of their geographical distance, should be treated as a panmictic population. Thi Loan et al. (2015) did not observe such a mitochondrial lineage divergence within the house-farm swiftlets, but suggested that the house-farm swiftlets could have originated from the southern region of Southeast Asia.

To answer our question, five of the cyt-b sequences published by Aowphol et al. (2008) and 11 by Thi Loan et al. (2015) were retrieved from GenBank and aligned with Hap3 and Hap6 (representing Clade 1) and Hap10 and Hap11 (representing Clade 2) obtained in this study (Table 4). In our own cyt-b data, five clade-specific sites were identified. However, the cyt-b regions used by Aowphol et al. (2008) and Thi Loan et al. (2015) covered only two and three clade-specific sites, respectively (Table 4, Fig. 2), suggesting that the two-clade pattern could possibly exist in the house-farmed swiftlet colonies in Thailand and Vietnam but undetected by both studies because of the choice of DNA markers.

Taxonomic identification of GenBank accessions depends entirely on the statement of the depositor, which may be open to error. We have pointed out, above, that the previous wrong application of the species name amechanus to house-farm specimens by two of the present authors led to misinterpretation by Rheindt et al. (2014). Rheindt et al. (2014) concluded that all white-nest swiftlets should be m

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357


Table 2. List of wild specimens collected, their locations and their mtDNA haplotypes which consists of cytochrome-b (1–817 bp) and NADH dehydrogenase 2 (818–1,213 bp).

Species Collection number Haplotype Location

A. fuciphagus vestitus LCK161703t, LCK161703u, LCK161703w, LCK161703x, LCK161703y, LCK161703z

Hap13 Middle Baram, Sawarak

LCK161703a, LCK161703cc Hap14 Middle Baram, Sawarak

LCK161703bb Hap15 Middle Baram, Sawarak

A. inexpectatus 162003f, 162003g Hap26 Pulau Seringgis, Terengganu

160314a (nest) Hap28 Balambangan Island, Sabah

A. maximus 162003b, 162003c, 162003d Hap18 Pulau Seringgis, Terengganu162003a Hap19 Pulau Seringgis, Terengganu162003e Hap23 Pulau Seringgis, Terengganu

160309a (nest) Hap24 Batu Putih, Sembilan Islands, Perak160309b (nest) Hap25 Batu Putih, Sembilan Islands, Perak

A. salanganus 161503a, 161503b, 161503c, 161503d, 161503e, 161503f, 161503h

Hap27 Balambangan Island, Sabah

Table 3. Population Pairwise FST comparison for the population pairs based on the geographical distribution of the house-farm swiftlets and the wild A. f. vestitus of Middle Baram. All sequences in Clade 2 form an individual population. FST values with boldfaced indicate significant at p = 0.05.

PopulationWest Coast Peninsular Malaysia

NE Peninsular Malaysia

East Coast Peninsular Malaysia

Central Peninsular Malaysia

Sarawak Sabah Clade 2

NE Peninsular Malaysia –0.02366

East Coast Peninsular Malaysia 0.00108 0.03057

Central Peninsular Malaysia –0.05039 0.01596 –0.06684

Sarawak –0.02439 0.04155 –0.15789 –0.03651

Sabah –0.03634 –0.03578 0.01818 0.00024 0.03035

Clade 2 0.84133 0.84370 0.80022 0.80785 0.76465 0.81811

Middle Baram (A. f. vestitus) 0.90874 0.89852 0.82044 0.83618 0.74278 0.86185 0.86895

Fig. 2. Schematic diagram of the mitochondrial cyt-b region sequenced in the previous and present studies. Dark bands on the grey strip indicate the location of the five clade-specific sites.

358


treated as a single species, for which the prior systematic name is Aerodramus fuciphagus. We have summarised the genetic evidence that justifies the original conclusion by Chasen (1931, 1935), on ecological grounds, that there are two Aerodramus swiftlets making white-nests, separated by habit including choice of nesting site. For these two species common and systematic names are grey-rumped swiftlet Aerodramus inexpectatus, habitually frequenting islands, maritime cliffs and coastal stacks, from the Andamans to the islands of Vietnam and (formerly) Hainan, China, and Brown-rumped Swiftlet A. fuciphagus, occupyng inland caves and grottoes in Sumatra and Borneo, and both inland and coastal nesting sites in Java and Nusa Tenggara Barat, Indonesia (cf. Chantler, 2005).

As shown above, in our region, spontaneous occupation of buildings by white-nest swiftlets, the presumed precedent for house-farming, occurred first in Singapore, possibly by swiftlets emigrating from Java (Chasen, 1939), followed by Peninsular Malaysian states. Yet, despite the fact that Brown-rumped swiftlets A. fuciphagus do not occur in Peninsular Malaysia, our phylogenetic analyses indicate that A. f. vestitus from the interior of Sabah and Sarawak (Medway, 1966), appears to be the closest wild relative of 21st century house-farm swiftlets throughout Malaysia from west to east.

The generic affinity of house-farm swiftlets as Aerodramus is indisputable but, on the present mitochondrial genetic evidence, they cannot confidently be identified as members of either of the two wild white-nest species (neither Aerodramus fuciphagus nor A. inexpectatus). Our study re-confirms the existence of two divergent clades among house-farm swiftlets, noted by Cranbrook et al. (2013), but, being based on mitochondrial genes, this new evidence does not permit a clear conclusion as to the origin of either of these two clades within the house-farm genotype. Given the undisputed historic evidence that house-farming began in Java, Indonesia, where Aerodramus fuciphagus is the only wild white-nest swiftlet species, it may be that, contrary to the conclusion of Cranbrook et al. (2013), all house-farm populations have descended from this common origin. Cranbrook et al. (2013) and Thi Loan et al. (2015) considered that the genetic difference between house-farm swiftlets and these wild species of white-nest swiftlets justified taxonomic separation. Given that opportunities may arise for genomic research using Next-generation Sequencing (NGS), this proposal now seems premature.

Behaviourally, house-farm white-nest swiftlets are now congenitally entrained to seek buildings as nest sites. Available evidence in Peninsular Malaysia confirms that swiftlets from house-farms have not occupied natural caves, even in limestone rich areas near Ipoh or Kuala Lumpur where caves abound. This small change in innate behaviour could be sufficient to create a barrier to genetic exchange, and might be genetically controlled. In effect, during the few decades since the first occupation of buildings was noted in Java in the 1880s, and later in Malaysia and Vietnam, the interaction between birds seeking artificial structures

as nesting sites and humans erecting buildings specifically designed to create suitable habitats, may have led to the rapid selection of new genotype(s). Clutton-Brock (1981: Preface) offered a working definition of ‘domestication’, as “the manner in which man has manipulated and changed the way of life...by the enfoldment of animals within human societies”. In these terms, since house-farm swiftlets represent an apparently novel genotype isolated by behaviour from any wild progenitor, these white-nest swiftlets can reasonably be described as “domesticated” (as by Ramji et al., 2013). For the first time in history, an opportunity exists to investigate the genetic process underlying a new avian domestication. We hope to continue to play a part in this new frontier of biological science.

ACKNOWLEDGMENTS

This project was partly funded by the Malaysian Ministry of Education Fundamental Research Grant Scheme (FRGS/2/2014/SG05/UTAR/02/2), and a UTAR Research Scholarship Scheme grant to W.S. Siew. The collection of genetic material in Malaysia was permitted by the Department of Wildlife and National Parks Peninsular Malaysia (PERHILITAN; JPHL&TN[IP]:100-34/1.24 Jld 8 and JPHL&TN.TR:80-1/38 BHG.2[12]), and by Sabah Biodiversity Council (Access license JKM/MBS.1000-2/2.JLD 4 [107]) and the Sabah Forestry Department (JPHTN/TP[FSP] 100-14/18/2/KLT.32[14]). International travel by Cranbrook was partly paid from funds granted by the Merdeka Award 2014, which also supplemented the field allowance of Siew. The authors gratefully acknowledge the generous pro bono contribution by Micropathology Ltd, in the form of laboratory facilities, staff time, travel expenses and other non-financial assistance. The authors also express their gratitude to house-farm owners and others for their willing cooperation in sample collection: Albert Tan, Allan Koay, Aw Tai Yong, Chew, Chuah Shy Poy, S.K. Fong, Jannet Chong Lee Yung, Goh Chin Choon, Liew Yoon Fatt, Hayati Mokhtar, Nik Mohd Hal bin Nik Abdullah, Pak Said, Pak Rafi, Mohd Saiful Mansor, Wan Izzuddin Sulaiman, Tan Kok Hong, Tan Seng Geok, Tan Yoke Tian, and Raphe Zevenbergen. We thank F. H. Sheldon, F.E. Rheindt, and an anonymous reviewer for their helpful comments in improving this manuscript.

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Table 4. Variable sites extracted from the cyt-b multiple sequence alignment. The five clade-specific sites are shaded. Prefix “EU” – published by Aowphol et al. (2008), “JN” – Thi Loan et al. (2015). Dot (“.”) denotes DNA base identical to that of the first row. Predicted clade numbers for the JN and EU individuals are indicated with “?”.

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Clade1 5 5 6 4 6 9 0 5 0

4 4 3 5 5 3 1 3 4 8

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genetic diversity among white-nest swiftlets of the genus ... · rocky marine stacks around the...

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