Genetic Population and Evolutionary Dynamics of the Angel Sharks, Squatina spp.

Once so abundant as to be called the ‘common’ angelshark, Squatina squatina has been extirpated from nearly the entirety of its historical range, from the eastern North Atlantic, to the Mediterranean Sea [International Union for the Conservation of Nature (IUCN) Red List: Critically Endangered]. The angelshark now only occurs in any abundance in the waters surrounding the Canary Islands. I present the first genetic assessment of the angelshark’s population dynamics and diversity from three locations within the Canary Islands archipelago: Gran Canaria, Tenerife, and Lanzarote. Using a suite of individual mitochondrial genome regions [Control region (CR), NADH dehydrogenase subunit 2 (ND2), NADH dehydrogenase subunit 4 (ND4), and Cytochrome c oxidase subunit 1 (COI)], the complete mitogenome, and nuclear markers [microsatellites and Internal Transcribed Spacer 2 (ITS2)] this work aimed to i) assess the genetic diversity of the angelshark in comparison to other endangered or historically overfished elasmobranchs, ii) examine the relative nucleotide variability across different marker sets, and iii) assess fine-scale multi-locus population structure within the Canary Islands, as well as broad-scale population genetic structure of angelsharks throughout its historic Eastern Atlantic and Mediterranean range. Results revealed exceptionally low genetic diversity across all individual mitochondrial regions sequenced (CR, π % = 0.0046 ± 0.016; ND2, π % = 0; ND4, π % = 0; COI, π % = 0), yielding some of the lowest values reported to date in any elasmobranch. Mitogenome analysis followed this low diversity trend with only 11 single nucleotide polymorphisms seen across all Canary Island individuals in a genome of 16,689 bp (π % = 0.0257 ± 0.0166). Furthermore, screening of 35 microsatellite markers across 34 individuals revealed all but two loci to be monomorphic and nuclear ITS2 showed negligible diversity. Lanzarote showed significant population differentiation from both Gran Canaria (ΦST = 0.073, p = 0.004, FST = 0.113, p = 0.00) and Tenerife (ΦST = 0.029, p = 0.001, FST = 0.065, p = 0.001) at the CR. Haplotype analysis of whole mitogenomes also demonstrated Lanzarote individuals forming a separate lineage from angelsharks at the other two islands. Broad- scale structure across the angelshark’s historical range was detected between the Canary Islands and Mediterranean (ΦST = 0.792, p = 0.000, FST = 0.785, p = 0.000), indicating a regional break between populations. The exceptionally low levels of genetic diversity in angelsharks in the Canary Islands, as well as indications of population isolation from the rest of the angelshark’s historical range, suggest an immediate need for strong conservation measures to ensure the protection and continued persistence of this highly vulnerable and ecologically unique species

A Genetic Exploration in a Last Refuge: The Common Angelshark (Squatina squatina) in the Canary Islands

The common angelshark (Squatina squatina) has been extirpated from nearly the entirety of its historical eastern North Atlantic and Mediterranean range and is listed as ‘Critically Endangered’ by the IUCN Red List of Threatened Species. Currently, only a single known remnant population of any abundance exists, occurring within the waters surrounding the Canary Islands. Nothing is known about the genetic population dynamics of this species. To assess the common angelshark’s genetic connectivity and diversity, tissue samples (n = 509) were collected between 2009-2016 from three separate islands within the archipelago: Gran Canaria and Tenerife – which are separated by a deep ocean channel (~3000 m) which potentially serves as a barrier to dispersal for this benthic species, and Lanzarote. To date, DNA sequences have been obtained from four mitochondrial loci [control region (CR) (n = 233), Cytochrome c oxidase subunit 1 (COI) (n = 16), NADH dehydrogenase subunit 4 (ND4) (n =28), and NADH dehydrogenase subunit 2 (ND2) (n =4)] revealing exceptionally low genetic diversity across all regions, as identical haplotypes were found in nearly all analyzed individuals. Additionally, next-generation sequencing has been used to develop a species-specific library for novel microsatellites and preliminary screening of each of 18 markers has shown these loci to be monomorphic across 16 individuals. Further screening of additional loci (mitochondrial and microsatellite) and individuals is ongoing. Such potentially low levels of genetic diversity may have far reaching implications for the persistence of this species and ultimately underscore the common angelsharks’ highly vulnerable state

The Complete Mitochondrial Genome of the Critically Endangered Angelshark, Squatina squatina

Here, we describe the first mitochondrial genome of the angelshark, Squatina squatina. The genome is 16,689 bp in length with 13 protein-coding genes, 22 tRNA genes, 2 rRNA genes, and a non-coding control region. Base composition of the mitogenome has an A + T bias (62.9%), seen commonly in other elasmobranchs. This genome provides a key resource for future investigations of the population genetic dynamics and evolution of this Critically Endangered shark

Almost Angels? The Critically Endangered Angelshark (Squatina squatina) in its Last Refuge, the Canary Islands

Once so abundant as to be called the ‘common’ angelshark, Squatina squatina has been extirpated from nearly the entirety of its historical range, from the eastern North Atlantic, to the Mediterranean (IUCN Red List Critically Endangered). The angelshark now seems to occur in any abundance only in the waters surrounding the Canary Islands. We present the first genetic assessment of the angelshark’s population dynamics and diversity. Tissue samples were collected between 2007-2016 from three islands within the archipelago: Gran Canaria, Tenerife, and Lanzarote. To investigate the genetic population dynamics, a three part approach was adopted: (i) DNA sequencing four mitochondrial regions commonly used in vertebrate population analysis [control region, COI, ND4, and ND2] of 300 angelsharks, (ii) Whole mitochondrial genome sequencing of nine individuals to identify and examine the comparative sequence variability in other gene regions, and (iii) assessment of nuclear diversity with 40 species-specific microsatellites. Results reveal exceptionally low genetic diversity across all individual mitochondrial regions sequenced, with single haplotypes in each region found across nearly all individuals. Mitogenome analysis follows this trend with only 11 single nucleotide polymorphisms seen across all Canary Island individuals in a genome of 16,689 bp. Furthermore, screening of 40 microsatellite markers across 32 individuals has shown all but two loci to be monomorphic. Such low levels of genetic diversity may have implications for the evolutionary persistence of this species and ultimately underscore the angelsharks’ highly vulnerable state