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19 May 2020 High Connectivity Among Breeding Populations of the Elegant Tern (Thalasseus elegans) in Mexico and Southern California Revealed Through Population Genomic Analysis
Gabriella S. Perez, Katharine S. Goodenough, Michael H. Horn, Robert T. Patton, Enrico A. Ruiz, Enriqueta Velarde, Andres Aguilar
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Abstract

Population genetic structure can aide in developing conservation and management strategies by characterizing populations on local and regional scales. The Elegant Tern (Thalasseus elegans) has a restricted breeding range, with a majority of its nesting population historically found on Isla Rasa, Gulf of California, Mexico. Since the late 1950s, increased frequency of low marine productivity due to warm oceanographic anomalies, such as El Niño events, have caused northward expansion of Elegant Tern breeding colonies into southern California, USA. To test the hypothesis that high gene flow occurs between Gulf of California and southern California Elegant Tern breeding colonies, restriction-site associated DNA sequencing was used to analyze 5,510 single nucleotide polymorphisms from 69 Elegant Terns sampled across four known breeding sites: Isla Rasa, Mexico (n = 30), San Diego National Wildlife Refuge, USA (n = 17), Bolsa Chica Ecological Reserve, USA (n = 11), and Port of Los Angeles, USA (n = 11). Analyses revealed little population subdivision, with non-significant genetic differentiation (FST) among sites and no geographic association of individuals, but there was subtle clustering of individuals by breeding site. These results suggest a strong degree of gene flow among the Gulf of California and southern California nesting colonies and indicate that Elegant Terns have a fluid breeding distribution and move readily among nesting sites.

Changes in species distributional patterns can provide valuable information on local, regional, and global responses to climate change and anthropogenic impacts (Pacifici et al. 2015; Beaugrand and Kirby 2018). Natural colonization of new habitats that lead to range expansions are useful instances to examine potential factors and consequence of species' range changes (Lenoir and Svenning 2015). Range expansions can lead to novel evolutionary and ecological adaptations to newly encountered environments (Rehm et al. 2015), and understanding of the underlying patterns and processes in these instances will be useful in projecting future conservation scenarios. From a conservation perspective, understanding the source/sink dynamics of newly colonized versus ‘core’ habitats can be informative in predicting the future persistence of all populations for a species, especially given current and predicted impacts of global climate change.

As top predators, seabirds are important links in food webs and are considered good environmental indicators of the health of marine ecosystems and abundance of prey species (Einoder 2009; Horn and Whitcombe 2015; Paleczny et al. 2015; Velarde et al. 2015). Fitness of seabirds is directly tied to populations of fish prey species (Velarde et al. 2015; Gomez-Laich et al. 2015; Cecere et al. 2015). Throughout the annual cycle, seabirds exploit a heterogeneous landscape (Cecere et al. 2015) and must take advantage of pulses in food availability to successfully breed, molt, and migrate. Generally, seabirds are colonial, long-lived, and exhibit pair-bonding. Most migrate after the nesting season and demonstrate high fidelity to nesting sites (Levin and Parker 2012; Clucas et al. 2016), but see Coulson (2016) who suggests a range of fidelity exists within seabird populations to counter seasonal variability in resources.

Of all bird groups, seabirds are the most imperiled, with 30% of Charadriiformes threatened with extinction (Paleczyny et al. 2015; Mancini et al. 2016). In addition to habitat loss and degradation, seabird populations are threatened by invasive species (e.g., rats), egging, diverse types of fisheries (i.e. as bycatch), and plastics pollution. These environmental challenges cause changes in breeding phenology (Wanless et al. 2009), and loss of suitable breeding and foraging habitats. In response to environmental challenges, some seabirds can change their patterns of migration and dispersal by expanding their foraging range (McLeay et al. 2010; Cecere et al. 2015), shifting breeding phenology, colonizing new breeding locations, or a combination thereof (Monaghan 1996; Velarde et al. 2015; Dayton et al. 2017).

The Elegant Tern (Thalasseus elegans) is included in the Mexico category of Special Protection for species that have a very restricted breeding distribution and are under risk of decline due to decades of intensive egg harvesting on Isla Rasa, Mexico (SEMARNAT 2010). In the United States, the tern is a species protected under the Migratory Bird Treaty Act of 1918, and