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Tursiops Aduncus T Durham Research Online Deposited in DRO: 20 September 2018 Version of attached le: Published Version Peer-review status of attached le: Peer-reviewed Citation for published item: Gridley, T. and Elwen, S. H. and Harris, G. and Moore, D. M. and Hoelzel, A. R. and Lampen, F. (2018) 'Hybridization in bottlenose dolphinsa case study of Tursiops aduncus T. truncatus hybrids and successful backcross hybridization events.', PLoS ONE., 13 (9). e0201722. Further information on publisher's website: https://doi.org/10.1371/journal.pone.0201722 Publisher's copyright statement: c 2018 Gridley et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Additional information: Use policy The full-text may be used and/or reproduced, and given to third parties in any format or medium, without prior permission or charge, for personal research or study, educational, or not-for-prot purposes provided that: • a full bibliographic reference is made to the original source • a link is made to the metadata record in DRO • the full-text is not changed in any way The full-text must not be sold in any format or medium without the formal permission of the copyright holders. Please consult the full DRO policy for further details. Durham University Library, Stockton Road, Durham DH1 3LY, United Kingdom Tel : +44 (0)191 334 3042 | Fax : +44 (0)191 334 2971 https://dro.dur.ac.uk RESEARCH ARTICLE Hybridization in bottlenose dolphinsÐA case study of Tursiops aduncus × T. truncatus hybrids and successful backcross hybridization events T. Gridley1*, S. H. Elwen2, G. Harris3, D. M. Moore4, A. R. Hoelzel4, F. Lampen3 1 Centre for Statistics in Ecology, Environment and Conservation, Department of Statistical Sciences, a1111111111 University of Cape Town, C/o Sea Search Research and Conservation NPC, Muizenberg Cape Town, South Africa, 2 Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, C/o a1111111111 Sea Search Research and Conservation NPC, Muizenberg Cape Town, South Africa, 3 The South African a1111111111 Association for Marine Biological Research, uShaka Sea World, Point, Durban, South Africa, 4 Department of a1111111111 Biosciences, Durham University, Durham, United Kingdom a1111111111 * [email protected] Abstract OPEN ACCESS Citation: Gridley T, Elwen SH, Harris G, Moore DM, The bottlenose dolphin, genus Tursiops is one of the best studied of all the Cetacea with a Hoelzel AR, Lampen F (2018) Hybridization in minimum of two species widely recognised. Common bottlenose dolphins (T. truncatus), bottlenose dolphinsÐA case study of Tursiops are the cetacean species most frequently held in captivity and are known to hybridize with aduncus × T. truncatus hybrids and successful species from at least 6 different genera. In this study, we document several intra-generic backcross hybridization events. PLoS ONE 13(9): e0201722. https://doi.org/10.1371/journal. hybridization events between T. truncatus and T. aduncus held in captivity. We demonstrate pone.0201722 that the F1 hybrids are fertile and can backcross producing apparently healthy offspring, Editor: Cheryl S. Rosenfeld, University of Missouri thereby showing introgressive inter-specific hybridization within the genus. We document Columbia, UNITED STATES that female F1 hybrids can reach sexual maturity at 4 yr and 3 mo of age, and can become Received: September 19, 2017 pregnant and give birth before being fully weaned. The information presented has implica- tions for understanding hybrid reticulation among cetacean species and practical implica- Accepted: July 20, 2018 tions for captive facilities housing either Tursiops species or hybrids thereof. Published: September 12, 2018 Copyright: © 2018 Gridley et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original Introduction author and source are credited. It is becoming increasingly clear that reticulation among species lineages is common [1], and Data Availability Statement: All relevant data are can even support the establishment of new species radiations [2]. In her 2009 review of hybrid- within the paper. The mtDNA sequences of Ta1 and ization events in marine mammals, BeÂrube [3], summarises that 53 putative hybridization Tt1 are available on GenBank, accession numbers events have been reported within Cetacea, of which 28 hybrids have been identified within MH733901 and MH733902 respectively. captive facilities. The evolutionary significance of hybridisation among cetacean species is not Funding: This research was supported in part by a yet clear [4], however a better understanding of this process can be facilitated through investi- Claude Leon Post Doctoral Fellowship to TG (www. gations of hybridisation events in captivity. leonfoundation.co.za) and National ResearchFoundation Fellowship to SE (www.nrf.ac. The bottlenose dolphin (Tursiops spp.) is one of the best studied of all the cetaceans. How- za/). Sea Search Africa Pty provided travel funding ever, there remains continued debate surrounding the number of Tursiops species recognised to TG (www.seasearch.co.za). The funders had no and the phylogenetic relationships between populations from which we have genetic PLOS ONE | https://doi.org/10.1371/journal.pone.0201722 September 12, 2018 1 / 15 Hybridization in bottlenose dolphins role in study design, data collection and analysis, information. In the past as many as 20 different Tursiops species were identified ([5] cited in decision to publish, or preparation of the [6]). In 1990, Ross and Cockcroft [6] re-assessed the genus Tursiops and recognised only T. manuscript.The author(s) GH and FL received no truncatus, with high degrees of morphological variation linked to clines in sea surface temper- specific funding for this work. The funder provided support in the form of salaries for authors as ate. More recently, genetic techniques in concert with morphological and osteological data, follows: Claude Leon Post Doctoral Fellowship to have helped to document variation in the genus at the species and population level (e.g. [7± TG, National Research Foundation Fellowship to 10]). A minimum of two bottlenose dolphin species; the common bottlenose dolphin T. trun- SE. Salaries from SAAMBR uShaka Sea World to catus and Indo-Pacific bottlenose dolphin T. aduncus, are now widely accepted [11]. A third GH and FL, but did not have any additional role in species, the Burrunan dolphin, T. australis has recently been proposed [12] and a subspecies T. the study design, data collection and analysis, is recognised from the Black Sea [13]. decision to publish, or preparation of the truncatus ponticus manuscript. The specific roles of these authors are Hybridisation in Tursiops has been investigated in areas where the species ranges overlap. articulated in the `author contributions' section. An early study in Taiwan based on mtDNA sequences found no evidence for introgression [8] between . and . , while a later study in that region using bi-parentally Competing interests: GH and FL are employees of T aduncus T truncatus uShaka Sea World. The authors TG and SE have inherited nuclear DNA markers (20 microsatellite DNA loci) also found no evidence for declared that no competing interests exist. This admixture between the two species [14]. Off Australia, mtDNA lineages were distinct [12, 15] does not alter our adherence to PLOS ONE policies and there was no evidence for admixture between T. truncatus and T. aduncus lineages even on sharing data and materials. when sympatric in coastal waters [16]. Although the Austral-Asian lineage of T. aduncus shows reciprocal monophyly with the South African T. aduncus lineage, they are both in the same lineage separate from T. truncatus based on a mitogenome phylogeny [9]. Estimated divergence time between T. truncatus and T. aduncus lineages was 790Ka, while the divergence between the two T. aduncus lineages was 327Ka. The divergence between these two species is relatively old within the wider delphinid radiation and while various studies have suggested polyphyly with this genus [9, 17±20], this is likely not fully resolved. All captive hybrids are within the odontocete suborder [3]. Common bottlenose dolphins (T. truncatus) are the most frequent cetacean to be housed in captive facilities and have hybrid- ized with species from 6 genera, including the rough toothed dolphin (Steno bredanensis), Gui- ana dolphin (Sotalia guianensis), Risso's dolphin (Grampus griseus) and false killer whale (Pseudorca crassidens) [3, 21±23]. Such events may reflect naturally occurring hybridization in areas where species distributions overlap, and there is strong evidence across a range of odon- tocete and mystecete cetaceans for such hybridization events in the wild [17, 24±28]. However, documentation of intra-generic hybridization events in captive or free-ranging Tursiops are rare, possibly due to prior confusion over the taxonomic status of this genus, difficulties in identifying hybrids in the wild using morphological features, or lack of overlap in species ranges limiting opportunities for mating. Alternatively, mechanisms of reproductive isolation may be in place which actively reduce the occurrence of hybridization events within Tursiops. Studies of free-ranging cetaceans
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