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Hybridization and Back-Crossing in Giant Petrels (Macronectes Giganteus and M

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Hybridization and Back-Crossing in Giant Petrels (Macronectes Giganteus and M RESEARCH ARTICLE Hybridization and Back-Crossing in Giant Petrels (Macronectes giganteus and M. halli) at Bird Island, South Georgia, and a Summary of Hybridization in Seabirds Ruth M. Brown1, N. M. S. Mareile Techow2, Andrew G. Wood1, Richard A. Phillips1* 1 Ecosystems Programme, British Antarctic Survey, Cambridge, United Kingdom, 2 Percy FitzPatrick Institute, DST/NRF Centre of Excellence, University of Cape Town, Cape Town, South Africa * [email protected] Abstract Hybridization in natural populations provides an opportunity to study the evolutionary pro- cesses that shape divergence and genetic isolation of species. The emergence of pre-mat- ing barriers is often the precursor to complete reproductive isolation. However, in recently diverged species, pre-mating barriers may be incomplete, leading to hybridization between OPEN ACCESS seemingly distinct taxa. Here we report results of a long-term study at Bird Island, South Georgia, of the extent of hybridization, mate fidelity, timing of breeding and breeding suc- Citation: Brown RM, Techow NMSM, Wood AG, Phillips RA (2015) Hybridization and Back-Crossing cess in mixed and conspecific pairs of the sibling species, Macronectes halli (northern giant in Giant Petrels (Macronectes giganteus and M. halli) petrel) and M. giganteus (southern giant petrel). The proportion of mixed-species pairs var- at Bird Island, South Georgia, and a Summary of ied annually from 0.4–2.4% (mean of 1.5%), and showed no linear trend with time. Mean Hybridization in Seabirds. PLoS ONE 10(3): laying date in mixed-species pairs tended to be later than in northern giant petrel, and al- e0121688. doi:10.1371/journal.pone.0121688 ways earlier than in southern giant petrel pairs, and their breeding success (15.6%) was Academic Editor: Hans-Ulrich Peter, Institute of lower than that of conspecific pairs. By comparison, mixed-species pairs at both Marion and Ecology, GERMANY Macquarie islands always failed before hatching. Histories of birds in mixed-species pairs at Received: February 11, 2013 Bird Island were variable; some bred previously or subsequently with a conspecific partner, Accepted: February 19, 2015 others subsequently with a different allospecific partner, and some mixed-species pairs re- Published: March 27, 2015 mained together for multiple seasons. We also report the first verified back-crossing of a hy- Copyright: © 2015 Brown et al. This is an open brid giant petrel with a female northern giant petrel. We discuss the potential causes and access article distributed under the terms of the evolutionary consequences of hybridization and back-crossing in giant petrels and summa- Creative Commons Attribution License, which permits rize the incidence of back-crossing in other seabird species. unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the Natural Environment Research Council (www.nerc.ac.uk). The funder had no role in study design, data collection and analysis, decision to publish, or Introduction preparation of the manuscript. Speciation, the process by which taxa evolve mechanisms conferring reproductive isolation, is Competing Interests: The authors have declared generally considered to occur when geographically isolated populations gradually acquire ge- that no competing interests exist. netic differences, either through selection or drift [1,2]. Reproductive isolation is achieved PLOS ONE | DOI:10.1371/journal.pone.0121688 March 27, 2015 1/14 Hybridization in Giant Petrels when genetic incompatibilities between sibling taxa become so great that offspring are infertile or unviable. If allopatric populations come into contact before this point is reached then there is the potential for interbreeding and genetic homogenization, unless behavioural isolating mechanisms, such as differences in the timing of breeding or incompatibility in mating dis- plays, are sufficient to maintain reproductive isolation [3]. However, pre-copulatory barriers are often incomplete, leading to hybridization and gene flow between seemingly distinct taxa, particularly where divergence was relatively recent [4–6]. The study of hybridization in natural populations therefore provides important insights into the processes of evolutionary diversifi- cation, as well as contributing to accurate identification of species boundaries. The two species of giant petrels are the only members of the genus Macronectes. Originally regarded as a single species, northern and southern giant petrels M. halli and M. giganteus, were spilt by Bourne & Warham [7] on the basis of morphological and behavioural differences, including the timing of breeding, colour of the bill tip and presence of a white morph in only one taxon (southern giant petrel). At some islands where the two species occur sympatrically there also appear to be differences in nest site selection [7,8]. Both species have a circumpolar breeding distribution; southern giant petrels breed both further north and further south than northern giant petrels, and are more widespread in the South Atlantic, whereas northern giant petrels are more common on islands around New Zealand (Fig. 1). The two species breed sym- patrically at five island groups: South Georgia, the Prince Edward Islands, Îles Crozet, Îles Ker- guelen and Macquarie Island (Fig. 1)[9–11], although only four breeding pairs of southern giant petrels have been recorded at Kerguelen, compared with around 1400 pairs of northern giant petrels [9]. The most recent estimates of global population sizes are 11,800 and 50,170 breeding pairs of northern and southern giant petrels, respectively [12,13]. Hybridization between northern and southern giant petrels has been reported at Marion Is- land, Macquarie Island and South Georgia (Bird Island). At Marion, unbanded mixed-species pairs were observed on eggs in the 1974/75 and 1976/77 breeding seasons, and a banded mixed- species pair (male southern giant petrel, female northern giant petrel) made at least eight breed- ing attempts between 1976/77 and 1995/96. Eggs were laid within the normal laying period for northern giant petrels but none hatched [14,15]. At Macquarie there is just one record of a breeding attempt by a mixed-species pair in the 1970/71 breeding season, which also failed be- fore hatching [16]. At Bird Island six breeding attempts by mixed-species pairs (male southern giant petrel, female northern giant petrel) were recorded between 1978/79 and 1980/81, and all six chicks fledged successfully. In addition, nine breeding attempts were recorded between male southern giant petrels and putative hybrid females, and four chicks from these pairings fledged successfully [17]. These studies suggest that hybridization between northern and southern giant petrels is both more prevalent and more successful at Bird Island than elsewhere. Systematic annual monitoring of ringed giant petrels of both species resumed at Bird Island in 2002/03. Using these data in combination with data collected between 1978/79 and 1980/81 by Hunter [17], we investigate various aspects of hybridization, including annual changes in the proportion of mixed-species pairs, timing of breeding, breeding success, and mate fidelity. We also report the first confirmed incidence of back-crossing between a hybrid and a northern giant petrel, summarise reports of hybridization in other seabird species, and discuss the poten- tial causes and consequences of hybridization and back-crossing in these taxa. Materials and Methods Ethics statement All animal work carried out during this study was conducted in accordance with UK Home Of- fice guidelines and all bird ringing was undertaken by licensed ringers. The species sampled are PLOS ONE | DOI:10.1371/journal.pone.0121688 March 27, 2015 2/14 Hybridization in Giant Petrels Fig 1. Breeding locations of northern (circles) and southern (triangles) giant petrels. Distribution data sourced from [9–11]. doi:10.1371/journal.pone.0121688.g001 not listed by CITES (Convention on the International Trade in Endangered Species). No per- mits were required for export of biological samples from South Georgia, and samples were im- ported into the UK under a DEFRA import licence (AHZ/2024A/2005/1). Fieldwork techniques involving live animals were approved by ethical review at the British Antarctic Survey. PLOS ONE | DOI:10.1371/journal.pone.0121688 March 27, 2015 3/14 Hybridization in Giant Petrels Annual monitoring Chicks and adults of both northern and southern giant petrels were ringed by various field par- ties at Bird Island, South Georgia (54°00'S, 38°03'W) during the breeding season (Sept. to April) in 1958/59–1963/64 and 1972/73–1973/74 and a detailed study of breeding biology and population dynamics was carried out in 1978/79–1980/81 [17–19]. Systematic monitoring of ringed giant petrels resumed at Bird Island in the breeding season of 2002/03. During the lay- ing period (late Sept.—early Dec.), a fixed study area of c. 28 hectares (c. 7% of the total area of the island) was checked at least weekly. All nests with an egg were marked with a wooden stake, the location recorded with a handheld GPS, and the nest visited weekly until the ring numbers of both incubating adults were recorded. Unringed adults were ringed during incuba- tion in the first season in which they bred. All adults in the study area were identified to species based on the colour of the endplate (or unguis) of the bill, which is dark red in northern giant petrels, and pale green in southern giant petrels. Breeding adults were sexed by visual examina- tion; males have a larger and deeper bill than females [20], and the accuracy of sexing checked by reference to the sex of the partner. From 2002/03 to 2004/05, nests were visited 2–3 times during the hatching period to con- firm successful hatching. Nests were visited again shortly before the fledging period, when the chicks were ringed and bill length recorded. From the start of the 2005/06 season, nests were visited every 1–2 days during laying in order to record laying dates, and then weekly thereafter to record dates of hatching and fledging, or failure date.
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