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Fine-scale genetic structure in Lahille’s bottlenose dolphins (Tursiops truncatus gephyreus) is associated with social structure and feeding ecology

Abstract

Varying levels of population structure may arise from interactions between intrinsic behavioral and demographic factors and extrinsic environmental factors. Social organization, habitat use, resource partitioning, or even individual preferences are putative drivers of population genetic differentiation over fine spatial scales. Here, genome-wide data from single-nucleotide polymorphisms (SNPs) and carbon and nitrogen stable isotope data were used to examine population structure and niche partitioning among three social units of bottlenose dolphins with strong home range overlap in a relatively small geographic area in southern Brazil. Results from model-based and model-free analyses of population structure supported the delineation of two populations, one with preferences for estuarine waters and another strictly coastal, consistent with isotopic niche differentiation. These findings suggest that genetic and ecological structuring is mainly driven by habitat use. At finer scale, we also detected low but significant genetic differentiation among the three social units. The outcomes of this study provide new insights into population structure of Lahille’s bottlenose dolphins in the Patos Lagoon estuary and its adjacent coastal waters, which are exposed to increasing levels of anthropogenic disturbances, such as intensive artisanal fisheries, pollution, and boat traffic. Although for demographic studies, the estuary and the coastal dolphins should be treated separately, for conservation purposes, we recommend that the three social units be regarded as different entities.

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Analysis reported in this article can be reproduced using the data provided in the Figshare repository: https://figshare.com/s/2ddb4f0b338f5437e280.

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Acknowledgements

We are very grateful to Cetacean Society International, Organization for the Conservation of South American Aquatic Mammals—YAQU PACHA e.V, Nuremberg Zoo, and Rancho Texas de Lancerote for funding support. The Coordination for the Improvement of Higher Education Personnel (CAPES) provided access to the Portal de Periódicos and financial support through Programa de Excelênca Acadêmica—PROEX. We also thank all field assistants for helping data collection over the years and Lauro Barcellos, director of the Oceanographic Museum ‘Prof Eliezer C. Rios’ at FURG, and NGO KAOSA for providing logistical support to the fieldwork. Jonathan Sandoval-Castillo provided useful advice in the data analysis and in the early drafts of the manuscript. Catherine Attard and Chris Brauer provided useful advice in the analysis development. Andrea Barceló, Minami Sasaki and Elisa Seyboth were important in the laboratory work. CNPq provided a research fellowship to E. R. S. (PQ 310597/2018-8). This article is part of RCG’s Ph.D. thesis in Biological Oceanography and was supported by the National Council for Scientific and Technological Development (CNPq—Brazil) and Yaqu Pacha (German) scholarships, and under a cotutelle agreement between Flinders University of South Australia and Universidade Federal do Rio Grande-FURG, under the supervision of E. R. S. and L. M. M. This agreement is within the scope of the Capes PrInt Program (public notice 041/2017). This study was part of the Brazilian Long Term Ecological Program (PELD—process 441492/2016-9), partially funded by CNPq (Ministry of Sciences, Technology, Innovation and Communication), and it is a contribution of the Research Group Ecologia e Conservação da Megafauna Marinha—EcoMega-FURG/CNPq. The funding was received by Conselho Nacional de Desenvolvimento Científico e Tecnológico (BR) (Grant nos. 403805/2012-0 and 41492/2016-9) and Cetacean Society International (US) (Grant no. 2014-8).

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Correspondence to Rodrigo Cezar Genoves.

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All applicable international, national and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. We only sampled adult animals and biopsy sampling procedures followed international guidelines, in accordance with ethical standards and under regional permits (Brazil’s SISBIO 24407-2, issued to P. F. F.). This article does not contain any studies with human participants performed by any of the authors.

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227_2019_3638_MOESM1_ESM.tif

Simulated mixing polygons for Lahille’s bottlenose dolphins sampled between 2009 and 2016 from A) the Patos Lagoon estuary social unit (PLE); B) the southern coast social unit (SC); and C) the northern coast social unit (NC). A set of trophic discrimination values for correcting prey isotopic values reported in Giménez et al. (2016) was applied. The position of the consumers (black dots) and the average source signatures (white crosses) are shown. Probability contours (black lines) are at the 5% level (outermost line) and at every 10% level. (TIF 371 kb)

227_2019_3638_MOESM2_ESM.tif

Relative contribution of prey sources to the diet of Lahille’s bottlenose dolphin units that use the Patos Lagoon estuary (PLE social unit), adjacent southern (SC social unit) and northern coasts (NC social unit) for six scenarios: Warm season (November – April) for PLE (A), SC (B), and NC (C) social units; Cold season (May – October; D) and period 2009-2012 (E) and period 2013-2016 (F) for PLE dolphins. Proportions of each fish species are shown as box plots showing 50%, 75% and 90% credibility intervals. Msp: Menticirrhus sp.; MF: Micropogonias furnieri; ML: Mugil liza; PB: Paralonchurus brasiliensis; TL: Trichiurus lepturus. (TIF 577 kb)

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Genoves, R.C., Fruet, P.F., Botta, S. et al. Fine-scale genetic structure in Lahille’s bottlenose dolphins (Tursiops truncatus gephyreus) is associated with social structure and feeding ecology. Mar Biol 167, 34 (2020). https://doi.org/10.1007/s00227-019-3638-6

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