Canadian Journal of Fisheries and Aquatic Sciences Genetic structure and congeneric range overlap among sharpnose sharks (Genus Rhizoprionodon) in the northwest Atlantic Ocean Journal: Canadian Journal of Fisheries and Aquatic Sciences Manuscript ID cjfas-2018-0019.R3 Manuscript Type: Article Date Submitted by the 10-Sep-2018 Author: Complete List of Authors: Davis, Matthew; Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute Suarez-Moo,Draft Pablo; Centro de Investigacion y de Estudios Avanzados del Instituto Politecnico Nacional, Unidad de Genómica Avanzada (Langebio) Daly-Engel, Toby; Florida Institute of Technology, Biological Sciences PHYLOGEOGRAPHY < General, SHARKS < Organisms, MOLECULAR Keyword: ECOLOGY < General, Rhizoprionodon, stock structure Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : https://mc06.manuscriptcentral.com/cjfas-pubs Page 1 of 33 Canadian Journal of Fisheries and Aquatic Sciences Genetic Structure in Rhizoprionodon 1 Genetic structure and congeneric range overlap among sharpnose sharks (Genus 2 Rhizoprionodon) in the northwest Atlantic Ocean 3 Matthew M. Davis1*,#1, Pablo de Jesus Suárez-Moo2, and Toby S. Daly-Engel3 4 1Department of Biology, University of West Florida, Pensacola, Florida, United States of 5 America 6 2Unidad de Genómica Avanzada (Langebio), Centro de Investigación y de Estudios Avanzados 7 del Instituto Politécnico Nacional, Irapuato, Guanajuato, Mexico 8 3Department of Biological Sciences, Florida Institute of Technology, Melbourne, Florida, United 9 States of America Draft 10 *Corresponding author 11 Email: [email protected] #1 New Address: Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, Cedar Key, Florida, United States of America Corresponding author contact: [email protected] https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 2 of 33 12 Abstract 13 Sharpnose sharks (Genus: Rhizoprionodon) experience extensive fishing pressure 14 throughout their ranges in the Atlantic Ocean, and as such it is important to understand the 15 degree to which intraspecific populations interact across a spatial gradient. The Atlantic 16 sharpnose shark Rhizoprionodon terraenovae and Caribbean sharpnose shark R. porosus share 17 similar appearance and spatial presence within the Gulf of Mexico (GOM), though previously 18 only R. terraenovae has been observed north of the Bahamas. We assessed the population 19 structure of R. terraenovae using the mitochondrial control region (650 bp). Our results indicate 20 significant genetic structure (FST = 0.049, P < 0.001; ΦST = 0.017, P = 0.008) between the GOM 21 and the rest of the Atlantic. In addition, Draftwe observed R. porosus outside their known range in 22 South Carolina, Virginia, and northern Florida. Given the overlapping range with R. terraenovae, 23 we assessed the potential for congeneric hybridization with the addition of the nuclear ribosomal 24 Internal Transcribed Spacer-2 gene (1260 bp). Results designate these specimens to be true R. 25 porosus specimens, indicating the need for reevaluation of this species’ range. https://mc06.manuscriptcentral.com/cjfas-pubs Page 3 of 33 Canadian Journal of Fisheries and Aquatic Sciences 26 Introduction 27 Elasmobranchs undergo direct development, allowing for dispersal at multiple life stages. 28 Though many large-bodied marine taxa such as sharks and billfishes have circumglobal 29 distributions and long-distance dispersal capabilities, research has shown many species can 30 exhibit genetic differentiation between small regional populations (Hellberg 2009; Clarke et al. 31 2015; Bernard et al. 2016; Williams et al. 2016). This is particularly evident in smaller coastal 32 sharks, such as the bonnethead Sphyrna tiburo (Fields et al. 2016), leopard shark Triakis 33 semifasciata (Barker et al. 2015), and blacknose shark Carcharhinus acronotus (Portnoy et al. 34 2014), where vagility is limited by body size (Musick et al. 2004). Population separation can be 35 attributed to a number of factors such asDraft strong surface currents, absence of continuous suitable 36 habitat, and geographic barriers, particularly between the Gulf of Mexico (GOM) and 37 northwestern Atlantic (Avise 1992; Portnoy et al. 2014; Portnoy et al. 2016). Additionally, many 38 sharks exhibit philopatry, relying on shallow coastal nursery habitat for parturition and 39 protection of neonates from larger predators (Holland et al. 1993; Carrier et al. 2004; Daly-Engel 40 et al. 2012). Species that exhibit natal philopatry and/or small home ranges may be more 41 vulnerable to local exploitation (Hueter et al. 2004), particularly if genetic subdivision between 42 populations is present but unaccounted for by management (Begg et al. 1999). 43 Members of the genus Rhizoprionodon are known for their ability to grow rapidly and 44 mature quickly (Loefer and Sedberry 2002). All Rhizoprionodon species are classified at the 45 level of “Least Concern” or “Data Deficient” by the International Union for the Conservation of 46 Nature (Cortés 2009). The Atlantic sharpnose shark Rhizoprionodon terraenovae is one of three 47 congeneric species in the western Atlantic Ocean, and the only one thought to occur north of the 48 Bahamas and Antilles, along the east coast of North America up to the Bay of Fundy, Canada 3 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 4 of 33 49 (Compagno 1984; Mendonça et al. 2011). The southern range of R. terraenovae overlaps in the 50 Bahamas with the northern range of its congener, the Caribbean sharpnose shark Rhizoprionodon 51 porosus (Mendonça et al. 2011). These two species are often mistaken for each other, as the only 52 known significant morphological difference is pre-caudal vertebral counts (R. terraenovae: 58- 53 66, R. porosus: 66-75; Springer 1964); however, molecular studies on mitochondrial and nuclear 54 DNA confirm that they are two distinct species (Mendonça et al. 2011). 55 Due to heavy prevalence of R. terraenovae in northwestern Atlantic ecosystems and 56 artisanal fisheries, several studies have examined its life history characteristics, such as 57 reproductive biology (Parsons 1983; Loefer and Sedberry 2002), age and growth (Parsons 1985; 58 Branstetter 1987; Loefer and Sedberry 2002; Frazier et al. 2015), and temporal changes in 59 distribution and abundance (Marquez-FaríDraftas and Castillo-Geniz 1998; Parsons and Hoffmayer 60 2005). Parsons and Hoffmayer (2005) assessed populations in the northern Gulf of Mexico from 61 March to October from 1998 to 2000, noting that the ratio of mature males to mature females 62 caught within the Mississippi Sound was immensely skewed (80:1), indicating that mature 63 females may predominantly remain nearshore or offshore. Additionally, a large decrease in 64 abundance of mature males during summer months was observed within Mississippi Sound, 65 possibly due to bioenergetically unfavorable conditions and/or migration to mate with females 66 (Parsons and Hoffmayer 2005). Similarly, no gravid females were caught inshore despite 67 consistent collection of neonate R. terraenovae with open umbilical scars, indicating that females 68 may give birth in nearshore waters, after which pups navigate to nursery grounds, an uncommon 69 trait in elasmobranchs (Parsons and Hoffmayer 2005). Given the stark segregation between sexes 70 and reliance of the pups on inshore nursery habitat, small-scale genetic structure in this 71 population may result from sex-biased dispersal. https://mc06.manuscriptcentral.com/cjfas-pubs Page 5 of 33 Canadian Journal of Fisheries and Aquatic Sciences 72 In addition to life history, several studies have focused on R. terraenovae molecular 73 ecology and large-scale genetic stock structure: Heist et al. (1996) first assessed the population 74 structure of R. terraenovae between Texas and Veracruz, Mexico, in the Gulf of Mexico and the 75 mid-Atlantic Bight using restriction fragment length polymorphisms (RFLPs), finding genetic 76 homogeneity between sites. Todd et al. (2004) investigated R. terraenovae genetic structure 77 between the southeast Atlantic and northern and southern Gulf of Mexico using single-stranded 78 conformational polymorphisms (SSCPs) from the mitochondrial genome, again finding no 79 significant genetic separation between sites. More recently, Suárez-Moo et al. (2013) amassed 80 samples from three proximate sites in the southeastern Gulf of Mexico, this time utilizing 81 amplified fragment length polymorphisms (AFLPs) to compare genetic structure; once again, 82 results indicated no significant populationDraft subdivision. Though these previous studies have not 83 shown genetic partitioning, we hypothesize that the use of highly polymorphic mtDNA 84 sequencing and large sample numbers from a variety of widely-separated locations could 85 uncover previously-unobserved genetic subdivision within or between biogeographic regions for 86 R. terraenovae, and possibly its congener R. porosus. 87 In recent years, observed range shifts for organisms in coastal ecosystems have increased 88 in frequency, possibly due to rising water temperatures (Perry et al. 2005; Stewart et al. 2014). 89 Given the similar external morphology in conjunction with overlapping ranges and life history 90 characteristics between R. terraenovae and R. porosus, landing records in the Atlantic may not 91 accurately