Abstract
In this study, Little Tern (Sternula albifrons) populations in Taiwan are examined based on two different types of data: mitochondrial control region DNA sequences and double digest restriction-site associated DNA (ddRAD) sequencing data. Feather samples were collected from 59 chicks across four known breeding colonies located on the eastern (Yilan and Hualien) and western (Penghu and Changhua) coasts of Taiwan. The results obtained are consistent in analyses and do not cluster into two geographical groups with respect to the eastern and western Taiwan. Furthermore, AMOVA analyses and pairwise ΦST/FST estimations based on both types of data reveal little to no differentiation among populations and between groups. The findings of this study suggest high population connectivity among Taiwan’s breeding colonies. Additionally, control region sequences of Taiwan’s Little Terns are compiled with those from Japan deposited in GenBank to compare genetic diversity and examine for phylogeographic breaks that could shape the diversity pattern of the species in eastern Asia. The resulting haplotype network does not clearly separate Taiwanese and Japanese populations, but the three most common haplotypes are prevalent for mainland Japan, Okinawa, and Taiwan. Little Tern populations may be frequently connected, but with some restrictions on gene flow causing moderate to great differentiation among the three. This is further supported by AMOVA analyses, pairwise ΦST estimations, and pattern of positive yet significant isolation by distance.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All mtDNA sequence data are deposited at NCBI GenBank under the following accession numbers: COI: OQ891693-OQ891743, and control region: OQ920922-OQ920978. ddRAD raw data are uploaded to the NCBI sequence read archive (SRA) under accession numbers SAMN34894844-SAMN34894893. There are no restrictions on data availability.
References
Abdul-Rahman F, Tranchina D, Gresham D (2021) Fluctuating environments maintain genetic diversity through neutral fitness effects and balancing selection. Mol Biol Evol 38:4362–4375. https://doi.org/10.1093/molbev/msab173
Andrew S (2010) FastQC: a quality control tool for high throughput sequence data. www.bioinformatics.babraham.ac.uk/projects/fastqc/. Accessed 28 Oct 2022
Andrews KR, Good JM, Miller MR et al (2016) Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet 17:81–92. https://doi.org/10.1038/nrg.2015.28
Antaky CC, Young L, Ringma J, Price MR (2021) Dispersal under the seabird paradox: probability, life history, or spatial attributes? Mar Ornithol 49:1–8
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300. https://doi.org/10.2307/2346101
Bertolero A, Oro D, Vilalta AM, López MÀ (2005) Selection of foraging habitats by Little Terns Sterna albifrons at the Ebro Delta (NE Spain). Revista Catalana D’ornitologia 21:37–42
Bicknell AWJ, Knight ME, Bilton D et al (2012) Population genetic structure and long-distance dispersal among seabird populations: implications for colony persistence. Mol Ecol 21:2863–2876. https://doi.org/10.1111/j.1365-294X.2012.05558.x
BirdLife Australia (2022) Little Tern. https://birdlife.org.au/bird-profile/little-tern. Accessed 7 Oct 2022
BirdLife International (2022) Species factsheet: Sternula albifrons. http://www.birdlife.org. Accessed 7 Oct 2022
BirdLife International (2022) Species factsheet: Sternula antillarum. http://www.birdlife.org. Accessed 15 Dec 2022.
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Boutilier ST, Taylor SA, Morris-Pocock JA et al (2014) Evidence for genetic differentiation among Caspian Tern (Hydroprogne caspia) populations in North America. Conserv Genet 15:275–281. https://doi.org/10.1007/s10592-013-0536-1
Byerly P, Chesser RT, Fleischer RC et al (2022) Museum genomics provide evidence for persistent genetic differentiation in a threatened seabird species in the western Atlantic. Integr Comp Biol 62:1838–1848. https://doi.org/10.1093/icb/icac107
Carlen E, Munshi-South J (2020) Widespread genetic connectivity of feral pigeons across the Northeastern megacity. Evol Appl 14:150–162. https://doi.org/10.1111/eva.12972
Catry T, Ramos JA, Catry I et al (2004) Are salinas a suitable alternative breeding habitat for Little Terns Sterna albifrons? Ibis 146:247–257. https://doi.org/10.1046/j.1474-919X.2004.00254.x
Chang L-N, Hung C-H, Yuan H-W (2013) Preliminary analysis of exploring the migratory pathways of the breeding Little Terns (Sternula albifrons) in Taiwan based on geolocator data (in Chinese). Department of Forestry and Resource Conservation, National Taiwan University, Taiwan
Cheng C-H (2007) Nest selection and reproductive ecology of terns in Huolong Beach and Xiaobaisha island, Penghu (in Chinese). Shagang Elementary School, Penghu County
Chiu TS, Young SS, Chen CS (1997) Monthly variation of larval anchovy fishery in I-lan bay, NE Taiwan, with an evaluation for optimal fishing season. J Fish Soc Taiwan 24:273–282
Clare M (2015) A Little Tern flagged in Taiwan visits Australia. https://www.10000birds.com/a-little-tern-flagged-in-taiwan-visits-australia.htm. Accessed 15 Dec 2022
Coulson JC (2016) A review of philopatry in seabirds and comparisons with other waterbird species. Waterbirds 39:229–240. https://doi.org/10.1675/063.039.0302
Cramer AN, Hoey JA, Dolan TE, Gatins R, Toy JA, Chancellor JL, Palkovacs EP, Garza JC, Beltran RS (2023) A unifying framework for understanding ecological and evolutionary population connectivity. Front Ecol Evol 11:1072825. https://doi.org/10.3389/fevo.2023.1072825
Crandall ED, Toonen RJ, Laboratory T, Selkoe KA (2018) A coalescent sampler successfully detects biologically meaningful population structure overlooked by F-statistics. Evol Appl 12:255–265. https://doi.org/10.1111/eva.12712
Crates R, Olah G, Adamski M et al (2019) Genomic impact of severe population decline in a nomadic songbird. PLoS ONE 14:1–19. https://doi.org/10.1371/journal.pone.0223953
Dayton J, Ledwoń M, Paillisson J et al (2017) Genetic diversity and population structure of the Eurasian Whiskered Tern (Clidonias hybrida hybrida), a species exhibiting range expansion. Waterbirds 40:105–117. https://doi.org/10.1675/063.040.0203
Draheim HM, Miller MP, Baird P, Haig SM (2010) Subspecific status and population genetic structure of Least Terns (Sternula anttilarum) inferred by mitochondrial DNA control-region sequences and microsatellite DNA. Auk 127:807–819. https://doi.org/10.1525/auk.2010.09222
Draheim HM, Miller MP, Baird P, Haig SM (2012) Temporal analysis of mtDNA variation reveals decreased genetic diversity in Least Terns. The Condor 114:145–154. https://doi.org/10.1525/cond.2012.110007
Dray S, Dufour A (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20
Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581. https://doi.org/10.1046/j.1365-294X.2002.01650.x
Earl DA, Vonholdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Eaton DAR, Overcast I (2020) Ipyrad: interactive assembly and analysis of RADseq datasets. Bioinformatics 36:2592–2594. https://doi.org/10.1093/bioinformatics/btz966
Eaton DAR, Ree RH (2013) Inferring phylogeny and introgression using RADseq data: an example from flowering plants (Pedicularis: Orobanchaceae). Syst Biol 62:689–706. https://doi.org/10.1093/sysbio/syt032
Erixon P, Svennblad B, Britton T, Oxelman B (2003) Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics. Syst Biol 52:665–673. https://doi.org/10.1080/10635150390235485
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491. https://doi.org/10.1093/genetics/131.2.479
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50. https://doi.org/10.1177/117693430500100003
Fagan WF, Meir E, Predergast J et al (2001) Characterizing population vulnerability for 758 species. Ecol Lett 4:132–138. https://doi.org/10.1046/j.1461-0248.2001.00206.x
Farmer B (2007) The albatross still looking for love after 40 years on the wrong side of the world. Mail Online. https://www.dailymail.co.uk/news/article-453705/The-albertross-looking-love-40-years-wrong-world.html. Accessed 15 Dec 2022
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Friesen VL (2015) Speciation in seabirds: why are there so many species and why aren’t there more? J Ornithol 156:27–39. https://doi.org/10.1007/s10336-015-1235-0
Fujii T, Kitamura W, Murofushi Y et al (2014) Australia Asia Little Tern Sternula albifrons geolocator project. Ornithol Sci 13:306
Fujita G, Totsu K, Shibata E et al (2009) Habitat management of Little Terns in Japan’s highly developed landscape. Biol Cons 142:1891–1898. https://doi.org/10.1016/j.biocon.2009.02.024
Gill F, Donsker D, Rasmussen P (eds) (2022) IOC world bird list (v12.2). https://www.worldbirdnames.org/bow/gulls/. Accessed 7 Oct 2022.
Gochfeld M, Burger J, Garcia EFJ (2020) Little Tern (Sternula albifrons), version 1.0. In Birds of the World (del Hoyo J, Elliott A, Sragatal J, Christie DA, de Juana E, Editors). Cornell Lab of Ornithology, Ithaca. https://doi.org/10.2173/bow.litter1.01
Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19
Goudet J (2005) Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186. https://doi.org/10.1111/j.1471-8286.2004.00828.x
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162. https://doi.org/10.1016/S0003-3472(80)80103-5
Greenwood PJ, Harvey PH (1982) The natal and breeding dispersal of birds. Annu Rev Ecol Syst 13:1–21
Habel JC, Zachos FE, Dapporto L, Rödder D, Radespiel U, Tellier A, Schmitt T (2015) Population genetics revisited—towards a multidisciplinary research field. Biol J Lin Soc 115:1–12. https://doi.org/10.1111/bij.12481
Hayakawa M, Suzuki-Matsubara M, Matsubara K et al (2022) Population genetic structure of Little Tern (Sternula albifrons) in Japan inferred from nucleotide sequence diversities of the mitochondrial DNA control region. Ornithol Sci 21:155–163. https://doi.org/10.2326/osj.21.155
Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004) Identification of birds through DNA barcodes. PLoS Biol 2:e312. https://doi.org/10.1371/journal.pbio.0020312
Higgins PJ, Davies SJJF (eds) (1996) Handbook of Australian, New Zealand and Antarctic Birds. Volume 3: Snipe to Pigeons. Oxford University Press, Melbourne
Huang G (2015) Breeding habitat use of Little Tern along Enshunada Coast-Tenryu River continuum in relation to dam development. J Environ Prot 6:204–214. https://doi.org/10.4236/jep.2015.63021
Hudson J, Castilla JC, Teske PR et al (2020) Genomics-informed models reveal extensive stretches of coastline under threat by an ecologically dominant invasive species. PNAS 118:e2022169118. https://doi.org/10.1073/pnas.2022169118
Hung C-H (2009) Factors affecting the hatching success of Little Terns in Lunwei Industrial Park (in Chinese). Unpublished master thesis, Department of Environmental Science and Engineering, Tunghai University, Taichung
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. https://doi.org/10.1093/bioinformatics/btm233
JNCC (2021) Little Tern (Sternula albifrons). https://jncc.gov.uk/our-work/little-tern-sternula-albifrons/. Accessed 7 Oct 2022
Johnston ASA, Boyd RJ, Watson JW, Paul A, Evans LC, Gardner EL, Boult VL (2019) Predicting population responses to environmental change from individual-level mechanisms: towards a standardized mechanistic approach. Proc R Soc B 286:20191916. https://doi.org/10.1098/rspb.2019.1916
Jombart T, Kamvar ZN, Collins C, et al (2020) Adegenet: exploratory analysis of genetic and genomic data. Data collection. The Comprehensive R Archive Network. https://cran.r-project.org/web/packages/adegenet/
Kamvar ZN, Tabima JF, Brooks JC (2018) Package ‘poppr’: genetic analysis of populations with mixed reproduction. https://cran.rproject.org/web/packages/poppr/poppr.pdf
Kersten O, Star B, Leigh D et al (2021) Complex population structure of the Atlantic puffin revealed by whole genome analyses. Commun Biol 4:922. https://doi.org/10.1038/s42003-021-02415-4
Kralj J, Martinovic M, Jurinovic L et al (2020) Geolocator study reveals east African migration route of Central European Common Terns. Avian Res 11:6. https://doi.org/10.1186/s40657-020-00191-z
Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Lee SL (2021) Suspected wild dogs invade Qingluo Wetland causing the Little Tern left early (in Chinese). Penghu Times. https://www.penghutimes.com/Article/Detail/1013. Accessed 15 Dec 2022
Leigh JW, Bryant D (2015) PopART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Lin DL, Pursner S (eds.) (2020) State of Taiwan’s birds. Endemic Species Research Institute, Taiwan Wild Bird Federation, Taiwan
Liu YQ (2021) Suspected wild dogs destroyed the nests and eggs of Little Terns causing an early end of breeding period in the important wetland in Penghu, Taiwan (in Chinese). Liberty Times Net. https://news.ltn.com.tw/news/life/breakingnews/3578207?fbclid=IwAR0EeRUyC56F5_OtqqoYu9Ap4iWYPXeQoYdkQuFshqAdd5uI7iQiHDF1ojA. Accessed 15 December 2022
Lois NA, Campagna L, Balza U et al (2020) Metapopulation dynamics and foraging plasticity in a highly vagile seabird, the southern rockhopper penguin. Ecol Evol 10:3346–3355
Lopes C, Ramos JA, Paiva VH (2015) Changes in vegetation cover explain shifts of colony sites of Little Terns (Sternula albifrons) in coastal Portugal. Waterbirds 38:260–268. https://doi.org/10.1675/063.038.0306
Lopez J, Nikolic N, Riethmuller M et al (2020) High genetic diversity despite drastic bottleneck in a critically endangered, long-lived seabird, the Mascarene Petrel Pseudobulweria aterrima. Ibis 163:268–273. https://doi.org/10.1111/ibi.12864
Mancilla-Morales MD, Velarde E, Aguilar A et al (2022) Strong philopatry, isolation by distance, and local habitat have promoted genetic structure in Heermann’s Gull. Diversity. https://doi.org/10.3390/d14020108
Manichaikul A, Mychaleckyj JC, Rich SS, Daly K, Sale M, Chen WM (2010) Robust relationship inference in genome-wide association studies. Bioinformatics 26:2867–2873
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
Marshall HD, Baker AJ (1997) Structural conservation and variation in the control region of fringilline finches (Fringilla spp.) and the greenfinch (Carduelis chloris). Mol Biol Evol 14:173–184. https://doi.org/10.1093/oxfordjournals.molbev.a025750
Martin CA, Armstrong C, Illera JC, Emerson BC, Richardson DS, Spurgin LG (2021) Genomic variation, population history and within-archipelago adaptation between island bird populations. R Soc Open Sci 8:201146. https://doi.org/10.1098/rsos.201146
Miller MR, Dunham JP, Amores A et al (2007) Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Res 17:240–248
Neigel JE, Avise JC (1986) Phylogenetic relationships of mitochondrial DNA under various demographic models of speciation. Evolutionary processes and theory. Academic Press, New York
NTU Biodiversity Center (2022) Report of the ecological survey and data collection on Taiwan seabird population 2020 (in Chinese). Biodiversity Research Center, National Taiwan University, Taiwan
Paleczny M, Hammill E, Karpouzi V, Pauly D (2015) Population trend of the world’s monitored seabirds, 1950–2010. PLoS ONE 10:e0129342. https://doi.org/10.1371/journal.pone.0129342
Pembleton LW, Cogan NOI, Forster JW (2013) stAMPP: an R package for calculation of genetic differentiation and structure of mixed ploidy level populations. Mol Ecol Resour 13:946–952. https://doi.org/10.1111/1755-0998.12129
Peng Y-W (2006) Population genetic structure of Steere’s Liocichla (Liocochla steerii) in Taiwan. Unpublished master thesis, Department of Forestry and Resource Conservation, National Taiwan University, Taiwan
Perez GS, Goodenough KS, Horn MH et al (2020) High connectivity among breeding populations of the Elegant Tern (Thalasseus elegans) in Mexico and southern California revealed through population genomic analysis. Waterbirds 43:17–27. https://doi.org/10.1675/063.043.0102
Peterson BK, Weber JN, Kay EH et al (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7:e37135. https://doi.org/10.1371/journal.pone.0037135
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1093/genetics/155.2.945
Pyle P, Hoffman N, Casler B, McKee T (2001) Little and Least Tern breeding on Midway Atoll: identification, range extensions, and assortative breeding behavior. North American Birds 55:3–6
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org.
Rajpar MN, Ozdemir I, Zakaria M et al (2018) Seabirds as bioindicators of marine ecosystems. Seabirds. IntechOpen, London. https://doi.org/10.5772/intechopen.75458
Rambaut A (2014) FigTree v1.4.2, a graphical viewer of phylogenetic trees. http://tree.bio.ed.ac.uk/software/figtree/
Ramírez O, Gomez-Díaz E, Olalde I et al (2013) Population connectivity buffers genetic diversity loss in a seabird. Front Zool 10:28. https://doi.org/10.1186/1742-9994-10-28
Renken RB, Smith JW (1995) Interior Least Tern site fidelity and dispersal. Colon Waterbirds 18:193–198. https://doi.org/10.2307/1521480
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228. https://doi.org/10.1093/genetics/145.4.1219
Safina C, Burger J, Gochfeld M, Wagner RH (1988) Evidence for prey limitation of Common and Roseate Tern reproduction. The Condor 90:852–859. https://doi.org/10.2307/1368842
Sandercock BK (2003) Estimation of survival rates for wader populations: a review of mark-recapture methods. Wader Study Group Bull 100:163–174
Sauve D, Patirana A, Chardine JW, Friesen VL (2019) Mitochondrial DNA reveals population genetic structure within Atlantic but not Pacific populations of a holarctic seabird, the Black-legged Kittiwake Rissa tridactyla. Mar Ornithol 47:199–208. https://doi.org/10.1111/j.1365-294X.2008.03977.x
Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337. https://doi.org/10.1007/s13127-011-0056-0
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Steiner UK, Gaston AJ (2005) Reproductive consequences of natal dispersal in a highly philopatric seabird. Behav Ecol 16:634–639. https://doi.org/10.1093/beheco/ari035
Suchan T, Espíndola A, Rutschmann S et al (2017) Assessing the potential of RAD-sequencing to resolve phylogenetic relationships within species radiations: the fly genus Chiastocheta (Diptera: Anthomyiidae) as a case study. Mol Phylogenet Evol 114:189–198. https://doi.org/10.1016/j.ympev.2017.06.012
Sunde J, Yıldırım Y, Tibblin P, Forsman A (2020) Comparing the performance of microsatellites and RADseq in population genetic studies: analysis of data for pike (Esox lucius) and a synthesis of previous studies. Front Genet 11:218. https://doi.org/10.3389/fgene.2020.00218
Szczys P, Lamothe KA, Druzyaka A et al (2017) Range-wide patterns of population differentiation of Eurasian Black Terns (Chlidonias niger niger) related to use of discrete post-nuptial staging sites. J Ornithol 158:365–378. https://doi.org/10.1007/s10336-016-1408-5
Teixeira JC, Huber CD (2021) The inflated significance of neutral genetic diversity in conservation genetics. PNAS 118:1–10. https://doi.org/10.1073/pnas.2015096118
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673
Thrasher DJ, Butcher BG, Campagna L et al (2018) Double-digest RAD sequencing outperforms microsatellite loci at assigning paternity and estimating relatedness: a proof of concept in a highly promiscuous bird. Mol Ecol Resour 18:953–965. https://doi.org/10.1111/1755-0998.12771
Walters AD, Schwartz MK, Rajora OP, Holenlohe PA (eds) (2020) Population genomics for the management of wild vertebrate populations. Population genomics: wildlife. Springer, Cham
Wang H-P (2022a) First breeding record of the Little Terns in Qigu, Tainan (in Chinese). Liberty Times Net. https://news.ltn.com.tw/news/life/breakingnews/3958547. Accessed 18 Jan 2023
Wang J (2022b) A joint likelihood estimator of relatedness and allele frequencies from a small sample of individuals. Methods Ecol Evol 13:2443–2462. https://doi.org/10.1111/2041-210X.13963
Weiser EL, Grueber CE, Jamieson IG (2013) Simulating retention of rare alleles in small populations to assess management options for species with different life histories. Conserv Biol 27:335–344. https://doi.org/10.1111/cobi.12011
Wernham CV, Toms MP, Marchant JH et al (2002) The migration atlas: movements of the birds of Britain and Ireland. T & AD Poyser, London
Whittier JB, Leslie DM, Van Den Bussche RA (2006) Genetic variation among subspecies of Least Tern (Sterna antillarum): implications for conservation. Waterbirds 29:176–184
Wright S (1943) Isolation by distance. Genetics 28:114–138
Wright S (1978) Variability within and among natural populations. Evolution and the genetics of populations 4. University of Chicago Press, Chicago
Zimmerman SJ, Aldridge CL, Oyler-McCance SJ (2020) An empirical comparison of population genetic analyses using microsatellite and SNP data for a species of conservation concern. BMC Genomics 21:382. https://doi.org/10.1186/s12864-020-06783-9
Acknowledgements
We thank the current and previous members from the Marine Biodiversity and Phylogenomics lab for help with molecular data collection and analysis during this study. We greatly appreciate Prof. Yu-Sheng Huang (National Penghu University of Science and Technology), committees of the Yilan and Hualien Bird Societies, and members (specially, Wei-Ting Chen) of Prof. Hsiao-Wei Yuan’s lab for help on the sampling permit application and field work. We are grateful to the MSK’s thesis committee members, Yu-Cheng Hsu (National Dong Hwa University), Si-Min Lin (National Taiwan Normal University), and Tzung-Su Ding (National Taiwan University), and the English editor, Buford Pruitt (wildlife biologist in US) for helpful comments and discussions on this work.
Funding
This project was supported by the National Science and Technology Council of Taiwan (NSTC110-2119-M-002-011 to WJC).
Author information
Authors and Affiliations
Contributions
Study conceptualization and experimental design: MSK and WJC; data collection: MSK and CHH; data analyses: MSK and LLH; first draft preparation: MSK; study supervision and revision of the manuscript: WJC; and resources: HWY.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interests.
Ethical approval
Sampling was performed under permission from consent authorities, and animal operations were approved by the Institutional Animal Care and Use Committee (IACUC) of National Taiwan University.
Consent to participate
Not applicable.
Consent for publication
All authors agree with the consent for publication.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Kong, M.S., Hung, CH., Hsu, LL. et al. Exploring genetic diversity and population structure of the Little Tern (Sternula albifrons) in Taiwan based on mtDNA and ddRAD sequencing data. Conserv Genet 25, 375–392 (2024). https://doi.org/10.1007/s10592-023-01574-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-023-01574-7