Abstract
The two species of yellow-nosed albatross, Atlantic (Thalassarche chlororhynchos) and Indian (T. carteri), are morphologically similar, but they differ in breeding behaviour and distribution. Both species are listed as endangered by the IUCN due to the limited number of breeding sites, threats from introduced predators and diseases, and impact of commercial fishing. We quantified genetic variation between and within the two species. Using nuclear (microsatellites and two nuclear sequences) and mitochondrial (control region) markers, we analysed 354 samples from four breeding islands (Atlantic: Nightingale, Inaccessible, and Gough; Indian: Amsterdam) and bycatch samples from South Africa and New Zealand. In addition to all markers separating the two species, nuclear markers showed Atlantic yellow-nosed albatrosses from Gough Island are genetically distinct from those breeding at Nightingale and Inaccessible Islands in the Tristan da Cunha archipelago. Nuclear markers confirmed that all bycatch samples were Indian yellow-nosed albatrosses, however, the bycatch birds from South Africa and New Zealand were distinct from each other and from birds breeding on Amsterdam Island, suggesting colony specific dispersal at sea. Our study supports the current recognition of two yellow-nosed albatross species and recognises genetically distinct groups of both Atlantic and Indian yellow-nosed albatross breeding on different islands, which is important for their conservation and management.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10592-021-01358-x/MediaObjects/10592_2021_1358_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10592-021-01358-x/MediaObjects/10592_2021_1358_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10592-021-01358-x/MediaObjects/10592_2021_1358_Fig3_HTML.png)
Similar content being viewed by others
Data availability
Sequencing and genotype data supporting the findings of this study are available at dryad and GenBank.
References
Abbott CL, Double MC (2003a) Phylogeography of shy and white-capped albatrosses inferred from mitochondrial DNA sequences: Implications for population history and taxonomy. Mol Ecol 12:2747–2758
Abbott CL, Double MC (2003b) Genetic structure, conservation genetics and evidence of speciation by range expansion in shy and white-capped albatrosses. Mol Ecol 12:2953–2962
Agreement on the Conservation of Albatrosses and Petrels (2009a) ACAP Species assessment: Indian yellow-nosed albatross Thalassarche carteri
Agreement on the Conservation of Albatrosses and Petrels (2009b) ACAP Species assessment: Atlantic yellow-nosed albatross Thalassarche chlororhynchos
Amaral AR, Beheregaray LB, Bilgmann K, Boutov D, Freitas L, Robertson KM, Sequeira M, Stockin KA, Coelho MM, Möller LM (2012) Seascape genetics of a globally distributed, highly mobile marine mammal: the short-beaked common dolphin (genus Delphinus). PLoS ONE 7:e31482
Angel A, Cooper J (2006) A review of the impacts of introduced rodents on the islands of Tristan da Cunha and Gough. Royal Society for the Protection of Birds, Sandy
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300
Bergek S, Björklund M (2007) Cryptic barriers to dispersal within a lake allow genetic differentiation of Eurasian perch. Evolution 61:2035–2041
BirdLife International (2018a) Thalassarche carteri. The IUCN Red List of Threatened Species 2018: e. T22728372A132657962. Downloaded on 20 September 2019
BirdLife International (2018b) Thalassarche chlororhynchos. The IUCN Red List of Threatened Species 2018: e.T22698425A132645225. Downloaded on 20 September 2019
Bried J, Dubois MP, Jouventin P, Santos RS (2008) Eleven polymorphic microsatellite markers in Cory’s shearwater, Calonectris diomedea, and cross-species amplification on threatened Procellariiformes. Mol Ecol Resour 8:602–604
Bugoni L, Mancini PL, Monteiro DS, Nascimiento L, Neves T (2008) Seabird bycatch in the Brazilian pelagic longline fishery and a review of capture rates in the southwestern Atlantic Ocean. Endanger Species Res 5:137–147
Burg TM (1999) Isolation and characterization of microsatellites in albatrosses. Mol Ecol 8:338–341
Burg TM, Croxall JP (2001) Global relationships amongst black-browed and grey-headed albatrosses: analysis of population structure using mitochondrial DNA and microsatellites. Mol Ecol 10:2647–2660
Clement M, Posada DCKA, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Coyne AE, Orr HA (2004) Speciation. Sinauer Associates, Sunderland
Cuthbert RJ, Cooper J, Ryan PG (2014) Population trends and breeding success of albatrosses and giant petrels at Gough Island in the face of at-sea and on-land threats. Antarct Sci 26:163–171
Dubois MP, Jarne P, Jouventin P (2005) Ten polymorphic microsatellite markers in the wandering albatross Diomedea exulans. Mol Ecol Notes 5:905–907
Earl DA, von Holdt BM (2012) Structure Harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Excoffier L, Lischer HE (2010) Arlequin suite version 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
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
Flood RL (2015) The two yellow-nosed albatrosses: molt, age, and identification. Birding 47:36–47
Friesen VL, Burg TM, McCoy KD (2007) Mechanisms of population differentiation in seabirds: Invited review. Mol Ecol 16:1765–1785
Gales R (1998) Albatross populations: status and threats. In: Robertson G, Gales R (eds) Albatross biology and conservation. Surrey Beatty & Sons, Chip** Norton
Gales R, Brothers N, Reid T (1998) Seabird mortality in the Japanese tuna longline fishery around Australia, 1988–1995. Biol Conserv 86:37–56
Geffen ELI, Anderson MJ, Wayne RK (2004) Climate and habitat barriers to dispersal in the highly mobile grey wolf. Mol Ecol 13:2481–2490
Inchausti P, Weimerskirch H (2002) Dispersal and metapopulation dynamics of an oceanic seabird, the wandering albatross, and its consequences for its response to long-line fisheries. J Anim Ecol 71:765–770
Jaeger A, Lebarbenchon C, Bourret V, Bastien M, Lagadec E, Thiebot JB, Boulinier T, Delord K, Barbraud C, Marteau C, Dellagi K, Tortosa P, Weimerskirch H (2018) Avian cholera outbreaks threaten seabird species on Amsterdam Island. PLoS ONE 13:e0197291
Jones MGW, Techow NMS, Risi MM, Jones CW, Hagens QA, Taylor F, Ryan PG (2020) Hybridisation and cuckoldry between black-browed and grey-headed albatrosses. Antarct Sci 32:10–14. https://doi.org/10.1017/S0954102019000506
Knutsen H, Jorde PE, André C, Stenseth NC (2003) Fine-scaled geographical population structuring in a highly mobile marine species: the Atlantic cod. Mol Ecol 12:385–394
Makhado AB, Crawford RJM, Dias MP, Dyer BM, Lamont T, Pistorius P, Ryan PG, Upfold L, Weimerskirch H, Reisinger RR (2018) Foraging behaviour and habitat use by Indian yellow-nosed albatrosses (Thalassarche carteri) breeding at Prince Edward Island. Emu 118:353–362
Moore PJ, Taylor GA, Amey JM (1997) Interbreeding of black-browed albatross Diomedea m. melanophris and New Zealand black-browed albatross D. m. impavida on Campbell Island. Emu 97:322–324
Múrias dos Santos A, Cabezas MP, Tavares AI, Xavier R, Branco M (2016) tcsBU: a tool to extend TCS network layout and visualization. Bioinformatics 32:627–628
Nunn GB, Stanley SE (1998) Body size effects and rates of cytochrome b evolution in tube-nosed seabirds. Mol Biol Evol 15:1360–1371
Nunn GB, Cooper J, Jouventin P, Robertson CJ, Robertson GG (1996) Evolutionary relationships among extant albatrosses (Procellariiformes: Diomedeidae) established from complete cytochrome-b gene sequences. Auk 113:784–801
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539
Penhallurick J, Wink M (2004) Analysis of the taxonomy and nomenclature of the Procellariiformes based on complete nucleotide sequences of the mitochondrial cytochrome b gene. Emu 104:125–147
Phalan B, Phillips RA, Double MC (2004) A white-capped albatross, Thalassarche [cauta] steadi, at South Georgia: first confirmed record in the south-western Atlantic. Emu 104:359–361
Phillips RA, Cooper J, Burg TM (2018) Breeding-site vagrancy and hybridization in albatrosses. Ibis 160:907–913
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rains D, Weimerskirch H, Burg TM (2011) Piecing together the global population puzzle of wandering albatrosses: genetic analysis of the Amsterdam albatross Diomedea amsterdamensis. J Avian Biol 42:69–79
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Rheindt FE, Austin JJ (2005) Major analytical and conceptual shortcomings in a recent taxonomic revision of the Procellariiformes—a reply to Penhallurick and Wink (2004). Emu-Austral Ornithol 105:181–186
Riginos C, Nachman MW (2001) Population subdivision in marine environments: the contributions of biogeography, geographical distance and discontinuous habitat to genetic differentiation in a blennioid fish, Axoclinus nigricaudus. Mol Ecol 10:1439–1453
Rolland V, Barbraud C, Weimerskirch H (2009) Assessing the impact of fisheries, climate and disease on the dynamics of the Indian yellow-nosed albatross. Biol Conserv 142:1084–1095
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Mol Biol Evol 34:3299–3302
Ryan PG, Dilley BJ, Ronconi RA (2019) Population trends of spectacled petrels Procellaria conspicillata and other seabirds at Inaccessible Island. Mar Ornithol 47:257–265
Silva MC, Duarte MA, Coelho MM (2011) Anonymous nuclear loci in the white-faced storm-petrel Pelagodroma marina and their applicability to other procellariiform seabirds. J Hered 102:362–365
Silva MC, Silva MF, Coelho MM (2012) Anonymous nuclear loci in Madeiran storm-petrel Oceanodroma castro (Procellariiformes: Hydrobatidae) and applicability across other procellariiform families. Conserv Genet Resour 4:1093–1095
Silva MC, Matias R, Wanless RM, Ryan PG, Stephenson BM, Bolton M, Ferrand N, Coelho MM (2015) Understanding the mechanisms of antitropical divergence in the seabird White-faced storm-petrel (Procellariiformes: Pelagodroma marina) using a multilocus approach. Mol Ecol 24:3122–3137
Steeves TE, Anderson DJ, Friesen VL (2005) A role for nonphysical barriers to gene flow in the diversification of a highly vagile seabird, the masked booby (Sula dactylatra). Mol Ecol 14:3877–3887
Sun Z, Elena G-D, Bailie A, Friesen V (2009) Isolation and characterization of microsatellite loci for storm-petrels. Mol Ecol Resour 9:913–915
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Taylor RS, Bolton M, Beard A, Birt T, Deane-Coe P, Raine AF, González-Solís J, Lougheed SC, Friesen VL (2019) Cryptic species and independent origins of allochronic populations within a seabird species complex (Hydrobates spp.). Mol Phylogenet Evol 139:106552
Viricel A, Rosel PE (2014) Hierarchical population structure and habitat differences in a highly mobile marine species: the Atlantic spotted dolphin. Mol Ecol 23:5018–5035
Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based ty** from forensic material. Biotechniques 10:506–513
Wanless RM, Angel A, Cuthbert RJ, Hilton GM, Ryan PG (2007) Can predation by invasive mice drive seabird extinctions? Biol Lett 3:241–244
Weimerskirch H (2004) Diseases threaten Southern Ocean albatrosses. Polar Biol 27:374–379
Weimerskirch H, Delord K, Fretwell PT, Marteau C, Ryan PG, Barbraud C (2018) Status and trends of albatrosses in the French Southern Territories, western Indian Ocean. Polar Biol 41:1963–1972
Wolfaardt AC, Glass J, Glass T (2009) Tristan da Cunha implementation plan for the Agreement on the Conservation of Albatrosses and Petrels (ACAP): review of current work and a prioritised work programme for the future. Tristan da Cunha Government, Tristan da Cunha
Wright S (1943) Isolation by distance. Genetics 28:114–138
Acknowledgements
We thank Henri Weimerskirch and Thierry Boulinier for providing samples from Amsterdam Island. Ben Dilley assisted with sample collection from Tristan da Cunha archipelago and Gough Island. Belinda Bauer, A Hewer and Tasmanian Museum and Art Gallery generously provided us samples. Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant, Alberta Innovates-Technology Futures Graduate Student Scholarship and the Seabird Group provided funding. Special thanks to members of Burg lab, University of Lethbridge for their enormous support.
Funding
Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant, Alberta Innovates-Technology Futures Graduate Student Scholarship, and the Seabird Group.
Author information
Authors and Affiliations
Contributions
PGR and TMB designed the study and PGR performed the fieldwork. ZWD and DKA completed the lab work and DKA led the analyses. DKA and TMB wrote the manuscript with input from the others.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
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
About this article
Cite this article
Abeyrama, D.K., Dempsey, Z.W., Ryan, P.G. et al. Cryptic speciation and population differentiation in the yellow-nosed albatross species complex. Conserv Genet 22, 757–766 (2021). https://doi.org/10.1007/s10592-021-01358-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-021-01358-x