Population structure of istiophorid billfishes

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Population structure of istiophorid billfishes John E. Graves ∗ , Jan R. McDowell Virginia Institute of Marine Science, College of William & Mary, 1375 Greate Rd., Gloucester Point, VA 23062, USA

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Article history: Received 28 March 2014 Received in revised form 13 August 2014 Accepted 27 August 2014 Available online xxx Keywords: Billfish Population structure Phylogeny

a b s t r a c t The phylogeny of istiophorid billfishes was recently revised based on analyses of nuclear and mitochondrial DNA loci, and a variety of molecular genetic characters has been used to investigate population structuring within several species of billfish. Despite these efforts, the population structure of most istiophorid billfishes is not well understood. This paper reviews genetic insights into the phylogeny and population structure of the billfishes with an emphasis on recent studies. In general, the results of genetic studies indicate significant heterogeneity between Atlantic and Indo-Pacific samples of circumtropical species. Within ocean basins, levels of population structure range among the species from no statistically significant heterogeneity detected among samples to small, but statistically significant genetic divergence between geographically distant samples. The apparent high level of genetic connectivity within oceans for some species seems to contrast with inferences derived from studies employing conventional and satellite tags that suggest limited trans-equatorial or trans-oceanic movements. This disparity may result, in part, from the different time scales underpinning evolutionary and ecological population structure; however, the power of previous genetic studies to elucidate population structuring has been limited by opportunistic sampling. To effectively assess population structure within the highly migratory billfishes, future genetic research will not only require larger sample sizes, both in terms of individuals and molecular markers, but also the development of biologically meaningful sampling designs that incorporate information on the movement patterns and life histories of these pelagic fishes. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Billfishes of the family Istiophoridae are pelagic fishes that occur throughout the world’s tropical and subtropical marine waters. The epipelagic environment in which they live is characterized by a lack of physical barriers, and the broad ranges and high dispersal abilities of these fishes tend to promote gene flow and erode population structure (Palumbi, 1994; Graves, 1998). NRM: In addition, most species are reported to spawn over broad geographic areas and over a prolonged season (Nakamura, 1985). The lack of barriers to gene flow in the epipelagic realm would be expected to limit genetic population structuring and speciation of the billfishes (Graves and McDowell, 2003). In fact, there are only nine extant species of istiophorid billfishes. Two species, the blue marlin (Makaira nigricans) and sailfish (Istiophorus platypterus), are distributed circumtropically, and three species, the black marlin (Istiompax indica), striped marlin (Kajikia audax), and shortbill spearfish (Tetrapturus angustirostris), are broadly distributed throughout the Pacific and Indian oceans. The white

∗ Corresponding author. Tel.: +1 804 684 7352; fax: +1 804 684 7157. E-mail address: [email protected] (J.E. Graves).

marlin (Kajikia albida), longbill spearfish (Tetrapturus pfluegeri), and roundscale spearfish (Tetrapturus georgii) occur throughout the Atlantic Ocean, while the Mediterranean spearfish (Tetrapturus belone) appears to be restricted primarily to the Mediterranean Sea. Billfishes are targeted in several small-scale artisanal fisheries, recreational fisheries, and represent a significant bycatch of pelagic longline fisheries for tunas and swordfish. Several species of billfishes are threatened by over-exploitation, especially the blue marlin and white marlin (Collette et al., 2011). A variety of techniques has been used to investigate population structuring within several species of billfish, with the majority of inferences resulting from studies using conventional tagging or genetic analyses. In general, these studies have demonstrated relatively low levels of population structuring, consistent with the high dispersal ability of these fishes in a relatively homogeneous epipelagic environment. The results of conventional tagging studies and genetic studies of billfishes were last reviewed at the Third International Billfish Symposium in 2001 (Ortiz et al., 2003; Graves and McDowell, 2003), and the taxonomy and phylogeny of istiophorid billfishes was revised at the Fourth International Billfish Symposium in 2005 (Collette et al., 2006). In this paper we consider those studies that have contributed to our understanding of billfish phylogeny and population structure since those reviews,

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Please cite this article in press as: Graves, J.E., McDowell, J.R., Population structure of istiophorid billfishes. Fish. Res. (2014), http://dx.doi.org/10.1016/j.fishres.2014.08.016

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and compare insights from population genetic analyses with those from conventional tagging studies. In addition, we consider factors that may be limiting insights gained from population genetic analyses, and provide recommendations for future studies.

2. Billfish phylogeny Nakamura (1985) recognized three genera and ten or eleven species within the Istiophoridae: Makaira comprised three species, the Atlantic blue marlin (M. nigricans), the Pacific blue marlin (M. mazara), and the black marlin (M. indica); Istiophorus consisted of two species, the Atlantic sailfish (I. albicans) and the Indo-Pacific sailfish (I. platypterus); and Tetrapturus was represented by five species, the striped marlin (T. audax), the white marlin (T. albidus), the shortbill spearfish (T. angustirostris), the longbill spearfish (T. pfleugeri), and the Mediterranean spearfish (T. belone), with the roundscale spearfish (T. georgii) being of questionable status. The validity of separate Atlantic and Indo-Pacific species of blue marlin and sailfish was questioned following genetic analyses that revealed minimal genetic divergence between ocean populations (Finnerty and Block, 1992; Graves and McDowell, 1995). Based on an analysis of three mitochondrial gene regions and a nuclear gene region, Collette et al. (2006) revised the Istiophoridae to include five genera and nine species. In the analysis, Makaira was not monophyletic and comprised two genera, Makaira and Istiompax. Makaira was represented by a single, circumtropical blue marlin (M. nigricans) that was sister to Istiophorus, and the placement of Istiompax, which comprised the black marlin (I. indica), was unstable. A single, circumtropical species of sailfish was recognized within Istiophorus (I. platypterus). Tetrapturus was also recognized as polyphyletic and considered to represent two monophyletic genera, Tetrapturus and Kajikia. Kajikia comprised two species, the striped marlin (K. audax) and the white marlin (K. albida), and Tetrapturus consisted of four species of spearfish: the shortbill spearfish (T. angustirostris), the longbill spearfish (T. pfleugeri), the Mediterranean spearfish (T. belone), and the roundscale spearfish (T. georgii), which was validated by Shivji et al. (2006). While there have not been any studies directly focused on the phylogeny of the Istiophoridae since the revision of Collette et al. (2006), the results of two recent genetic studies of billfishes can be used to evaluate their hypotheses. Hanner et al. (2011) reported on a mitochondrial DNA (mtDNA) barcoding study of istiophorid and xiphiid billfishes. They sequenced the mitochondrial COI gene region from 296 individuals, and included an additional 57 sequences from the literature. They also sequenced the nuclear rhodopsin gene for 72 individuals. Their results for both the COI and rhodopsin analyses supported the splitting of Makaira into Makaira and Istiophorus as well as the division of Tetrapturus into Tetrapturus and Kajikia. Analyses of these gene regions also reinforced the close genetic relationships of striped and white marlin within Kajikia, and the four spearfishes within Tetrapturus (Graves and McDowell, 1995; Collette et al., 2006). Consistent with the results of previous studies, neither gene region was able to resolve the species within either of these genera. Within Kajikia, 91 CO1 sequences, 44 from white marlin and 28 from striped marlin, resulted in 21 distinct haplotypes. Sequences from the two species were very similar; the between-group mean Kimura 2-parameter distance was 0.004 and in one case, the two species shared an identical haplotype (sequence). Results based on sequencing of the nuclear rhodopsin gene region, which included 22 striped marlin and 9 white marlin, had a single fixed nucleotide position that discriminated the majority of white and striped marlin; however, four striped marlin appeared to be heterozygous at this nucleotide position. Within Tetrapturus, 64 samples including 11 shortbill spearfish, 15 Mediterranean spearfish, 51 roundscale spearfish and

43 longbill spearfish COI sequences were examined resulting in 16 haplotypes, three of which were shared by two of the three species (Mediterranean + longbill, 2 shared haplotypes; Mediterranean + shortbill, 1 shared haplotype). Sequencing of rhodopsin from 27 samples including 10 roundscale spearfish, 7 longbill spearfish, 8 Mediterranean spearfish and two shortbill spearfish also failed to resolve these species. However, it is important to note that neither the COI nor the rhodopsin locus are known to be highly variable and therefore, given that billfishes are an evolutionarily recent group, examination of markers with a higher mutation rate is warranted. The second study by Bernard et al. (2013) surveyed sequence variation at a more variable mitochondrial ND4L-ND4 gene region to investigate the distribution of roundscale spearfish within the Atlantic Ocean. Their analysis included sequences from other species of istiophorid billfishes and the topology of the resulting maximum likelihood tree was consistent with that of Collette et al. (2006). As with previous studies, neither white and striped marlin nor longbill and Mediterranean spearfish were resolved. This study did not include shortbill spearfish samples. More research is needed to fully resolve the phylogeny of the Istiophoridae. The placement of Istiompax relative to the other genera remains problematic. White marlin and striped marlin are genetically very similar (Graves, 1998; Graves and McDowell, 2003) and were not resolved by Collette et al. (2006), Hanner et al. (2011), or Bernard et al. (2013). Similarly, there is a lack of resolution among the four spearfishes. Analysis of other gene regions as well as broader geographic sampling of specimens will be required to better understand these relationships.

3. Billfish population structure Blue Marlin: The blue marlin has a circumtropical distribution, primarily occupying waters with surface temperatures above 24 ◦ C (Nakamura, 1985). Little information is available regarding the spatial and temporal distribution of spawning, although larvae have been collected over broad areas in the Pacific and Atlantic oceans (Nakamura, 1985). Howard and Ueyanagi (1965) reported on spawning of blue marlin and other istiophorids throughout the Pacific Ocean, and several studies have provided insights into the temporal occurrence of blue marlin larvae at specific locations including the Great Barrier Reef, Australia (Leis et al., 1987), Hawaii (Hyde et al., 2005), Exuma Sound, Bahamas (Serafy et al., 2003), Bermuda (Luckhurst et al., 2006), and the northern Gulf of Mexico (Rooker et al., 2012). Conventional tagging studies demonstrate that blue marlin are capable of very high dispersal. Trans-oceanic and trans-equatorial movements have been documented within the Pacific and Atlantic oceans, and two tag recoveries have indicated movements between oceans (Ortiz et al., 2003). Analysis of minimum travel distance versus time at large revealed no apparent cyclical annual movements or site fidelity. Recently, Kraus et al. (2011) reported relatively restricted movements of blue marlin in the Gulf of Mexico based on results from pop-up satellite archival tags. Mean displacement in this study (588 km) was consistent with the results of conventional tagging studies (757 km; Orbesen et al., 2008), however, most of the observed movement involved seasonal north-south displacement. Fish tagged in the western Gulf of Mexico moved from the shelf edge off Texas and adjacent offshore waters in the summer to the shelf edge and adjacent offshore area at the U.S.–Mexico border during spring and fall, and were found in the central region of the Bay of Campeche during the winter months. This suggests the possibility that connectivity between the Gulf of Mexico and the rest of the North Atlantic Ocean may be limited. This is corroborated by the results of conventional tagging

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that indicate that only 0.047% of fish tagged in the North Atlantic Ocean were recaptured in the Gulf of Mexico (Orbesen et al., 2008). The genetic basis of blue marlin population structure was summarized by Graves and McDowell (2003). Analyses of nuclear and mitochondrial markers indicate slight, yet significant levels of divergence between Atlantic and Pacific populations, but provide no evidence of structuring within oceans. The results are consistent with either current low levels of gene flow between ocean basins, or the occurrence of gene flow in the recent past. However, two distinct mtDNA lineages, which differed by a net nucleotide sequence divergence of more than 1% based on RFLP of the whole mtDNA using 12 restriction enzymes and 5.17% based on 850 bp of the mtDNA control region, were found. The presence of these two mtDNA lineages, one of which was restricted to the Atlantic, suggests historical isolation of Atlantic and Pacific populations. Recently, Sorenson et al. (2013) evaluated the utility of genetic analyses to discriminate between Atlantic and Pacific blue marlin samples as a means to enforce a United States law that prohibits the importation of Atlantic blue marlin. They used 13 microsatellite loci as well as an allele-specific polymerase chain reaction assay designed to discriminate “Atlantic” and “ubiquitous” mtDNA lineages. Analysis of 187 Atlantic and 157 Pacific samples from geographically distant collection locations within each ocean revealed low, but statistically significant genetic divergence (FST = 0.01, P < 0.05) across Atlantic and Pacific samples. Consistent with the results of previous studies, the Atlantic mitochondrial lineage occurred in 40.6% of Atlantic blue marlin; however, it was also noted in a single Pacific blue marlin (0.64% of Pacific samples). A more detailed analysis of blue marlin population structure within the Atlantic was performed by McDowell et al. (2007), who surveyed nucleotide sequence variation at the mtDNA control region in 57 blue marlin caught in four widely separated sampling locations during the 1997–1998 calendar year; the western North Atlantic (n = 15), the Caribbean Sea (n = 11), the western South Atlantic (n = 13) and the eastern Atlantic (n = 18). High levels of genetic variation were found within each collection; 54 of the 57 samples had unique haplotypes, but there was no evidence of statistically significant population structuring within the Atlantic Ocean (P = 0.96). Conventional tagging studies have demonstrated high dispersal of blue marlin and no evidence of seasonal site fidelity, and these results are consistent with those of genetic analyses. There is no evidence at this time to support genetically-based stock structure of blue marlin within the Pacific or Atlantic oceans, and there is little information on blue marlin from the Indian Ocean. Small, but significant divergence exists between Atlantic and Pacific ocean populations, suggesting recent isolation or current low levels of gene flow. The documentation of two inter-ocean movements suggests the potential for current gene flow between ocean populations. However, the suggestion that connectivity between the Gulf of Mexico and the rest of the North Atlantic Ocean may be limited based on satellite tags points to the need for further study. Sailfish: The sailfish, like the blue marlin, has a circumtropical distribution, and spawning is reported to occur over a broad temporal and spatial range (Nakamura, 1985). In contrast to the large displacements noted for some blue marlin, conventional tagging data reveal relatively limited dispersal of sailfish. No trans-oceanic or trans-equatorial movements have been noted for sailfish in either the Atlantic or Pacific Ocean, and analysis of minimum travel distance versus time at liberty data suggests that in some areas sailfish either undergo cyclical seasonal movements, and/or exhibit site fidelity (Ortiz et al., 2003). Sailfish, like blue marlin, exhibit low, but significant genetic divergence between Atlantic and Pacific populations, with two distinct mtDNA lineages occurring in the Atlantic, one of which also occurs in the Pacific (Graves and McDowell, 2003). The divergence

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between the two mtDNA lineages (0.65% based on RFLP analysis of an 1800 bp fragment including the mtDNA control region using 12 restriction endonucleases and 2.6% based on sequencing of an 871 bp fragment of the mtDNA control region) is a bit lower than that reported between Atlantic and Pacific blue marlin (1.23% and 5.17%, respectively), but, as with blue marlin, is consistent with historical isolation. The presence of individuals with identical “ubiquitous” lineage haplotypes in both oceans suggests either current, limited gene flow, or recent isolation. Genetic analyses have not demonstrated population structuring of sailfish within the Atlantic Ocean. McDowell and Graves (2002) surveyed genetic variation at three nuclear microsatellite loci and mtDNA for 293 sailfish from six locations throughout the Atlantic Ocean and were unable to reject the null hypothesis of a single stock. In contrast, significant structuring has been documented within the Pacific Ocean. Hoolihan et al. (2004) reported a distinct stock of sailfish within the Arabian Gulf based on restriction analysis of an 1800 bp region of the mtDNA that included the control region using eight restriction enzymes. Analysis of 139 individuals from the Arabian Gulf and Indian Ocean found significant differences between samples taken inside and outside the Arabian Gulf (FST = 0.356) and reduced haplotype diversity in the Gulf was consistent with a founder effect. It is important to note that this study used 8 restriction endonucleases that were found to be variable in a preliminary analysis, therefore the magnitude of differences are not directly comparable to (are inflated as compared to) other studies which did not pre-select restriction endonucleases. Similarly, McDowell (2002) reported significant genetic heterogeneity among sampling locations within the Pacific and Indian oceans based on both analysis of the mtDNA control region and three microsatellite loci. Analysis of 353 Indo-Pacific sailfish using three microsatellite loci found that eastern and western Pacific samples were significantly different (FCT = 0.018, P < 0.001) but that western Pacific samples were not significantly different from samples taken in the Indian Ocean when excluding samples collected in the Persian Gulf (FCT = 0.00, P = 0.34). As with the Hoolihan et al. (2004) study, samples from the Persian Gulf were significantly different from those taken from other locations in the Indian Ocean (FST 0.022–0.036, P < 0.01). Recently, Lu and colleagues (this volume) have demonstrated significant heterogeneity between western North Pacific and eastern North Pacific sailfish using analyses of microsatellite loci and mtDNA gene regions. Relative to other istiophorid species for which there are large conventional tagging databases, sailfish exhibit the lowest levels of dispersal (Ortiz et al., 2003), and this is reflected in the genetically based population structure. Like blue marlin, there is low but significant population structuring between the Atlantic and Indo-Pacific sailfish. However, in contrast to the larger, more vagile blue marlin, sailfish also exhibit significant heterogeneity within the Indian and Pacific oceans, and additional research is needed to better understand the stock structure of sailfish in these regions, as well as to further explore structuring within the Atlantic. Black Marlin: The black marlin is broadly distributed in the warmer waters of the Pacific and Indian oceans (Nakamura, 1985). Spawning is known to occur seasonally in the South China Sea, around Taiwan, and off the Great Barrier Reef (Nakamura, 1985). The major conventional tagging effort for black marlin has occurred off the Great Barrier Reef and results have shown that the species is capable of great dispersal: trans-equatorial, trans-oceanic, and inter-oceanic movements (from the Pacific to the Indian Ocean) have been documented. Plots of minimum travel distance versus time at large for conventional tags suggest that black marlin exhibit cyclical annual movements or seasonal site fidelity (Ortiz et al., 2003). Recent pop-up satellite archival tagging of adult black marlin off the Great Barrier Reef during the spawning season provided insights on movements of individuals for up to six months following

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the spawning season and demonstrated that the spawning aggregation has a catchment area that extends up to 5000 km from the spawning area (Domeier and Speare, 2012). Little is known of the genetic basis of black marlin stock structure. Preliminary studies employing restriction site analysis of the mtDNA control region and analysis of three microsatellite loci could not reject the null hypothesis of a single Pacific stock (Falterman, 1999). Recently, Chen et al. (unpublished data) analyzed nucleotide sequence data from two mtDNA gene regions and demonstrated significant genetic heterogeneity among 178 black marlin sampled from six Indo-Pacific collection locations. Continued sampling and genetic analyses will provide better insights to the population structure of a billfish species that is known to undertake extensive movements. Striped Marlin: Striped marlin, like black marlin, are distributed in the Pacific and Indian oceans, with major abundance occurring in a horseshoe shaped distribution centered on the coast of Central America in the Pacific Ocean (Nakamura, 1985). Spawning, as evidenced by the occurrence of ripe individuals and larvae, is known to occur during seasons of a few months at several locations in the Pacific and Indian oceans (Howard and Ueyanagi, 1965; Nakamura, 1985; Hyde et al., 2006; Kopf et al., 2012). Conventional tagging studies (reviewed in Ortiz et al., 2003) have demonstrated trans-equatorial movements of striped marlin, and while many long distance movements have been noted within the Pacific, complete trans-oceanic movements have not been demonstrated. Unlike some species of billfish, conventional tagging data provide little evidence of site fidelity or cyclical annual movements of striped marlin. Studies using pop-up satellite archival tags (PSATs) have provided additional insights about regional movements in the eastern North Pacific (Domeier, 2006) and western South Pacific (Sippel et al., 2011). Domeier (2006) deployed 248 PSATs on striped marlin over 5 years at several locations throughout the Pacific Ocean including Baja California, Mexico; the Galapagos Islands and Salinas, Ecuador; southern California and Hawaii, USA; the southeast tip of Australia and northern New Zealand. Results indicated striped marlin exhibit some degree of regional site fidelity; little to no mixing was observed between fish tagged at different regions during the course of study. In addition, striped marlin tagged near the edge of their geographic range were found to have longer distance movements than those tagged near the center of their range; fish tagged off Mexico had a mean straight-line-distance of 480 km as compared to 2500 km for fish tagged off New Zealand. There was also evidence of seasonal movements based on these data, one fish tagged off New Zealand moved 2000 km before returning to within 400 km of the tagging location eight months later. A second PSAT study by Sippel et al. (2011) deployed 28 tags on striped marlin between the years 2005–2008 in the southwest Pacific. They noted that striped marlin halted their northward movement when they reached a latitude of 20–21◦ S, with many of the fish changing direction and moving back south. Although the oceanographic variables triggering this behavior are unknown, this finding is consistent with a known break in the distribution of striped marlin in the central and western Pacific (Squire and Suzuki, 1990). Relative to the other istophorid billfishes, striped marlin exhibit the greatest degree of genetic population structuring. Genetic analyses employing nuclear and mitochondrial molecular markers demonstrated significant heterogeneity among collection locations within the Pacific Ocean (reviewed in Graves and McDowell, 2003). Subsequently, McDowell and Graves (2008) surveyed variation of mtDNA control region sequences and five microsatellite loci in 373 striped marlin collected at seven locations within the Pacific Ocean including Taiwan and Japan in the northwest Pacific; Port Stephens, Australia in the southwest Pacific; Kona, Hawaii in the central North

Pacific; Cabo San Lucas, Mexico and San Diego, California in the northeast Pacific; and Manta, Ecuador in the southeast Pacific. Analysis of these samples based on microsatellites revealed significant population structure. In pairwise comparisons, FST values ranged from a non-significant value of 0.004 (P = 0.435) between samples taken in California and Japan to a value of 0.0276 (P < 0.001) between Mexico and Australia. The global FST among all samples was 0.0134 (P < 0.001). Four distinct stocks were delineated based on microsatellites in this study: north Pacific (California, Hawaii, Japan and Taiwan), Mexico, Ecuador, and Australia, which correspond to the four known striped marlin spawning areas. The mtDNA results demonstrated the same trend as the microsatellites, there was a non-random association between mtDNA sequence similarity and geographic location. In a later, more comprehensive study, which included both mature and immature samples taken from Hawaii, Purcell and Edmands (2011) surveyed variation in 1199 striped marlin from seven Pacific locations (Japan, Hawaii, Southern California, Mexico, Central America, New Zealand, and Australia), analyzing mtDNA control region sequences and 12 microsatellite loci. Both the microsatellite and mtDNA analyses revealed significant heterogeneity. Based on microsatellites, the global FST among all samples was 0.0145, and FST values based on pairwise comparisons in this study ranged from 0.0013 (P > 0.05) between southern California and Japan to 0.0374 (P < 0.001) between Mexico and Australia. Four groups of fish were delineated, southwest Pacific (Australia and New Zealand) eastern Pacific (Mexico and Central America), north Pacific (Japan, Southern California, and immature Hawaii) and mature Hawaii. In general, there was agreement between the stock structure inferred from analyses of the two classes of markers, and with the previous results of McDowell and Graves (2008). The most intriguing result of this study was the finding of significant differences between mature and immature fish collected in Hawaii FST = 0.0066, P < 0.001, suggesting that distinct stocks may use this area during different life history stages. The relatively high degree of genetic population structuring of striped marlin observed in the Pacific Ocean by independent analyses would suggest limited movements or some type of seasonal site fidelity. However, conventional tagging data do not support either scenario. The situation is enigmatic and continued population structure analyses employing both genetic and electronic tagging technologies will be required to better understand striped marlin stock structure. For genetic analyses, this should include the addition of Indian Ocean samples as well as multiple life history stages. White Marlin: White marlin are distributed throughout the tropical and subtropical Atlantic Ocean (Nakamura, 1985). Spawning is reported to occur in a broad area through the tropics, (Nakamura, 1985), and regional studies have provided insights into spawning seasons in particular regions (Prince et al., 2005; Arocha and Bárrios, 2009; Rooker et al., 2012). Conventional tagging of white marlin has occurred primarily in the western North Atlantic (reviewed in Ortiz et al., 2003) and results demonstrate considerable movements within that region. Trans-oceanic movements have been noted, but there have been no reports of trans-equatorial movements. Analysis of minimum travel distances and time at large for fish at liberty for up to 15 years suggest cyclical annual movements and seasonal site fidelity (Ortiz et al., 2003). In their review of billfish genetic stock structure, Graves and McDowell (2003) reported no significant heterogeneity among white marlin sampling locations throughout the Atlantic Ocean based on mtDNA restriction analysis of the whole mtDNA molecule. Subsequently, Graves and McDowell (2006) surveyed sequence variation at the mtDNA control region and variation at five microsatellite loci for 214 white marlin from three western Atlantic and one eastern Atlantic location. Results from the mtDNA

Please cite this article in press as: Graves, J.E., McDowell, J.R., Population structure of istiophorid billfishes. Fish. Res. (2014), http://dx.doi.org/10.1016/j.fishres.2014.08.016

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and microsatellite markers were not completely consistent and although F-statistics approached statistical significance (0.0163, P = 0.069 and 0.0022, P = 0.057, respectively), neither analysis revealed significant overall heterogeneity. Pairwise comparisons of geographic collections resulted in one significant comparison for each class of marker, although the results were not consistent between the mtDNA and microsatellite markers. For microsatellites, western North Atlantic samples taken off the U.S. mid-Atlantic coast were significantly different from western South Atlantic samples taken off Brazil (FST = 0.0041, P = 0.017). Analysis of mtDNA control region sequences indicated that western north Atlantic samples differed significantly from those taken off the Dominican Republic and Venezuela in the Caribbean Sea (˚ST = 0.040, P = 0.045). The genetic data are not inconsistent with the tagging data, which suggest the possibility of a cyclical seasonal patterning to the movements of white marlin. Overall, the results of this study suggest that if white marlin do exhibit genetic stock structure, the signal is weak compared to the congeneric striped marlin and delineation will likely require larger sample sizes, a more biologically meaningful sampling design, and higher resolution genetic methods. Spearfishes: There is little information available on the population structure of the spearfishes. These tend to be the rarest of the billfish species (Nakamura, 1985) and obtaining representative samples throughout a species’ range has been problematic. Furthermore, the species-level (alpha) taxonomy of the group is not well resolved, and species identification is difficult, especially in some areas of the eastern North Atlantic where three species may occur sympatrically (Robins, 1974; Nakamura, 1985). In recent years several studies have investigated the distribution of the roundscale spearfish, which is morphologically similar to the white marlin. The roundscale spearfish was originally described from a single individual caught off the island of Madeira (Lowe, 1840), but there were concerns about the validity of the species (Robins and de Sylva, 1960). A morphological analysis of eastern North Atlantic istiophorids by Robins (1974) supported the existence of the roundscale spearfish and suggested that it was restricted to the eastern North Atlantic. Shivji et al. (2006) used genetic techniques to validate the roundscale spearfish, and confirmed its presence in the western North Atlantic. Subsequent genetic and morphological studies have demonstrated that the relative abundance of roundscale spearfish and white marlin can vary dramatically in the western North Atlantic, and have expanded the range of roundscale spearfish into the western South Atlantic (Beerkircher et al., 2008; Arocha and Silva, 2010; Graves and McDowell, 2012; Bernard et al., 2013).

4. Challenges and opportunities There are many challenges to investigating the population structure of the istiophorid billfishes, and none is more formidable than collecting representative samples. Relative to other pelagic species such as tunas and swordfish, istiophorid billfishes are rare. There are very few directed billfish fisheries, and a large fraction of global landings result from bycatch in high seas pelagic longline fisheries that target tunas and swordfish. Consequently, obtaining robust collections of billfish from various locations throughout a species’ range is difficult. In general, researchers have concentrated their sampling efforts on those locations where there has been a reasonable probability of obtaining large numbers of individuals from local commercial or recreational fisheries. However, little attention has been given to sampling in areas where there are no directed fisheries or lower catch rates, obtaining multiple (seasonal) collections at one location, or to the sex or age composition of collections.

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As a result, the informational content of any particular sample within a collection is relatively low. Conventional tagging studies have clearly demonstrated that istiophorid billfishes are highly migratory, but analyses of minimum distance traveled versus time at large has suggested seasonal cyclical movements, or possible site fidelity, for some species (Ortiz et al., 2003). Thus, the physical presence of an individual in one location at a given time, especially if there is no seasonal stratification of samples, may not be particularly informative. Recent studies using PSATs to study movements and habitat utilization of billfishes have provided new insights into the nature and timing of billfish movements. For example, light-based geolocation analysis of a white marlin tagged with a PSAT during the fall of 2011 off the mid-Atlantic coast of the United States, indicated that the fish travelled south, well offshore of the continental shelf and outside of the Caribbean Sea, and spent the winter months off northern Brazil. In the spring the fish moved north and into the Caribbean (a known spawning area and season for white marlin) before returning north to waters offshore of the U.S. mid-Atlantic the following summer. After exactly 12 months, the tag popped up a few hundred km from the point of release (Fig. 1; Loose and Graves, unpublished data). Depending on the time of year, this fish could have been included in a U.S. mid-Atlantic collection, a northern Brazil collection, or a Caribbean collection. Understanding a species’ biology is critical to developing an appropriate sample design to test for population structure. Failure to do so can lead to incorrect conclusions. The Atlantic bluefin tuna provides an instructive example. Based on the existence of discrete spawning locations in the Mediterranean Sea and Gulf of Mexico and geographically separated fisheries in the eastern Atlantic and western Atlantic, eastern and western stocks were recognized (reviewed in Fromentin and Powers, 2005). While conventional tagging demonstrated some trans-Atlantic movements of bluefin, these were believed to occur at a low frequency. Early genetic studies of eastern and western bluefin typically included juveniles and adults of several age classes, and were unable to discriminate between the putative stocks (Edmunds and Sammons, 1973; Thompson and Contin, 1979; Broughton and Gold, 1997; Takagi et al., 1999; Ely et al., 2002; Pujolar et al., 2003). Subsequently, results from electronic tagging studies (Block et al., 2001, 2005; Wilson et al., 2005), otolith stable isotope analyses (Rooker et al., 2008), and investigations of tissue organochlorine pollutant ratios (Dickhut et al., 2009) provided new perspectives on movements of bluefin tuna between the western and eastern North Atlantic. Large numbers of juvenile bluefin tuna, 1 to 3 years of age, migrate from the eastern Atlantic to the western Atlantic, at times exceeding the abundance of native western juveniles in the western Atlantic. There is widespread movement of older year classes across the Atlantic, with apparent spawning site fidelity. To test for population structure, one should sample putative stocks at the time they are likely to be separated (Graves et al., 1996; Carlsson et al., 2004). For bluefin tuna, to effectively sample “true” eastern or western fish, one should target either spawning adults in the Gulf of Mexico and Mediterranean Sea, and/or youngof-the-year juveniles that are sufficiently small (young) that it is unlikely that they could have transited the North Atlantic. Studies that incorporated such a sampling design have demonstrated low, but highly significant levels of genetic heterogeneity between eastern and western bluefin tuna (Carlsson et al., 2007; Boustany et al., 2008), structure that was not evident with opportunistic sampling. Unfortunately, our understanding of the biology of any of the istiophorid billfishes is not as great as our understanding of the biology of Atlantic bluefin tuna, and that poses a major impediment to developing effective sample designs. Nevertheless, future studies would be well advised to consider the potential effects of season as well as age class and sex composition of their collections. While

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Fig. 1. Movement of a white marlin (Kajikia albida) during the course of one year inferred from light-based geolocation analysis (Loose and Graves, unpublished data). Depending on the time of year, this individual could have been included in collections from several different geographically distant sampling locations.

it may be logistically difficult to obtain large numbers of spawning adults from a single location, collection of early life history stages may offer another means to survey the genetic composition at a spawning location. Alternately, as more information becomes available through electronic tagging studies, it may be possible to design collection strategies that focus on sampling geographically distant feeding locations during the same season. Aside from the difficulties of collecting biologically meaningful samples, a major hindrance to advances in our understanding of the relationships among billfishes and the genetic basis of stock structure has been the limited number of molecular markers available for study. Fortunately, the advent of massively parallel sequencing has largely ameliorated this problem. For example, an Illumina HiSeq 2500 is capable of producing 30–40 Gb of sequence in a single lane (Illumina Inc., San Diego, CA) at relatively low cost (for a review of available sequencing platforms and their relative strengths, see Glenn (2011) and the accompanying yearly updates e.g. http://www.molecularecologist.com/next-gen-fieldguide-2014/). The high-throughput capacity of these machines means that the generation of large numbers of molecular markers, and even whole genomes, for non-model organisms is relatively inexpensive. In addition, an assortment of next generation sequencing-based approaches have been developed for population genetics, conservation genetics and phylogenetics, including methods that

target a reduced portion of the genome for sequencing, such as reduced representation libraries (RRLs) (Baird et al., 2008) and probe capture (Mamanova et al., 2010). RRL methods commonly use restriction enzymes in conjunction with adaptors and include methods such as RAD-seq (Davey et al., 2013) and genotyping-bysequencing (Narum et al., 2013). Probe capture methods can be tailored to pull out the portion of the genome of interest including capture of exons, transcriptomes, ultra-conserved elements (McCormack et al., 2012) and arrays of known loci (Bi et al., 2012). Although each of these methods has unique strengths and weaknesses, they all have great promise for increasing the fraction of the genome that is surveyed. This will clearly advance our understanding of billfish phylogeny, and the resulting increase in molecular markers available for population analyses will undoubtedly improve the power of those studies. However, to fully utilize the benefits of increased genomic sampling to population structure studies of istiophorid billfishes, a better understanding of the basic life history of these highly vagile species is required to formulate biologically meaningful sample designs. Acknowledgments We would like to thank Nadya Mamoozadeh and two anonymous reviewers for their insightful and constructive comments on

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