Comparative population genetics and evolutionary history of two commonly misidentified billfishes of management and conservation concern

BMC Genetics

Kevin A Feldheim³  Andres Domingo²  Freddy Arocha⁶  Fabio HV Hazin¹  Eric D Prince⁵  Mahmood S Shivji⁴  Andrea M Bernard⁴ 

[1] Departamento de Pesca e Aquicultura, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos, Recife 52171-032, PE, Brazil;Laboratorio de Recursos Pelágicos, Dirección Nacional de Recursos Acuáticos, Constituyente 1497, Montevideo 11200, CP, Uruguay;The Field Museum of Natural History, Pritzker Laboratory for Molecular Systematics and Evolution, 1400 South Lake Shore Drive, Chicago 60605, IL, USA;The Guy Harvey Research Institute, Oceanographic Center, Nova Southeastern University, 8000 N. Ocean Drive, Dania Beach 33004, FL, USA;National Marine Fisheries Service, Southeast Fisheries Science Center, 75 Virginia Beach Drive, Miami 33149, FL, USA;Instituto Oceanográfico de Venezuela, Universidad de Oriente, Apartado de Correos, 204, Cumaná 6101, Venezuela

关键词: Kajikia albida;    Tetrapturus georgii;    Effective population size;    Genetic diversity;    Genetic population structure;    White marlin;    Roundscale spearfish;   

Others  :  1085002
DOI  :  10.1186/s12863-014-0141-4

 received in 2014-07-01, accepted in 2014-12-01,  发布年份 2014

【 摘 要 】

Background

Misidentifications between exploited species may lead to inaccuracies in population assessments, with potentially irreversible conservation ramifications if overexploitation of either species is occurring. A notable showcase is provided by the realization that the roundscale spearfish (Tetrapturus georgii), a recently validated species, has been historically misidentified as the morphologically very similar and severely overfished white marlin (Kajikia albida) (IUCN listing: Vulnerable). In effect, no information exists on the population status and evolutionary history of the enigmatic roundscale spearfish, a large, highly vagile and broadly distributed pelagic species. We provide the first population genetic evaluation of the roundscale spearfish, utilizing nuclear microsatellite and mitochondrial DNA sequence markers. Furthermore, we re-evaluated existing white marlin mitochondrial genetic data and present our findings in a comparative context to the roundscale spearfish.

Results

Microsatellite and mitochondrial (control region) DNA markers provided mixed evidence for roundscale spearfish population differentiation between the western north and south Atlantic regions, depending on marker-statistical analysis combination used. Mitochondrial DNA analyses provided strong signals of historical population growth for both white marlin and roundscale spearfish, but higher genetic diversity and effective female population size (1.5-1.9X) for white marlin.

Conclusions

The equivocal indications of roundscale spearfish population structure, combined with a smaller effective female population size compared to the white marlin, already a species of concern, suggests that a species-specific and precautionary management strategy recognizing two management units is prudent for this newly validated billfish.

【 授权许可】

   
2014 Bernard et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Palumbi SR: Genetic divergence, reproductive isolation and marine speciation. Annu Rev Ecol Syst 1994, 25:547-572.
• [2]Waples RS: Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 1998, 89:438-450.
• [3]Theisen TC, Bowen BW, Lanier W, Baldwin JD: High connectivity on a global scale in the pelagic wahoo, Acanthocybium solandri (tuna family Scombridae). Mol Ecol 2008, 17:4233-4247.
• [4]Hauser L, Carvalho GR: Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 2008, 9:333-362.
• [5]Riccioni G, Landi M, Ferrara G, Milano I, Cariani A, Zane L, Sella M, Barbujani G, Tinti F: Spatio-temporal population structuring and genetic diversity retention in depleted Atlantic bluefin tuna of the Mediterranean Sea. Proc Natl Acad Sci U S A 2010, 107:2102-2107.
• [6]Knutsen H, Olsen EM, Jorde PE, Espeland SH, André C, Stenseth NC: Are low but statistically significant levels of genetic differentiation in marine fishes 'biologically meaningful'? A case study of coastal Atlantic cod. Mol Ecol 2011, 20:768-783.
• [7]Anonymous: Report of the 2011 blue marlin stock assessment and white marlin data preparatory meeting, Madrid, Spain April 25–29, 2011 Coll Vol Sci Papers ICCAT 2011, 68:1273-1386.
• [8]Collette B, Amorim AF, Bizsel K, Boustany A, Carpenter KE, de Oliveira Leite Jr N, Die D, Fox W, Fredou FL, Graves J, Viera Hazin FH, Hinton M, Juan Jorda M, Masuti E, Minte Vera C, Miyabe N, Nelson R, Oxenford H, Restrepo V, Schratwieser J, Teixeira Lessa RP, Pires Ferreira Travassos PE: Kajikia albida: IUCN Red List of Threatened Species. Version 2013.2. [http://www.iucnredlist.org/details/170322/0]
• [9]Collette BB, Carpenter KE, Polidoro BA, Juan-Jordá MJ, Boustany AM, Die DJ, Elfes C, Fox W, Graves J, Harrison LR, McManus R, Minte-Vera CV, Nelson R, Restrepo V, Schratwieser J, Sun C-L, Amorim A, Brick Peres M, Canales C, Cardenas G, Chang S-K, Chiang W-C, De Oliveira Leite Jr N, Harwell H, Lessa R, Fredou FL, Oxenford HA, Serra R, Shao K-T, Sumaila R, et al.: High value and long life - double jeopardy for tunas and billfishes. Science 2011, 333(6040):291-292.
• [10]ICCAT (International Commission for the Conservation of Atlantic Tunas): ICCAT Report for the biennial period, 2012 – 13, Part I – volume 2, Madrid, Spain ICCAT 2013, 2:119-130.
• [11]Shivji M, Magnussen JE, Beerkircher LR, Hinteregger GF, Lee DW, Serafy JE, Prince ED: Validity, identification, and distribution of the roundscale spearfish, Tetrapturus georgii (Teleostei: Istiophoridae): morphological and molecular evidence. Bull Mar Sci 2006, 79:483-491.
• [12]Beerkircher LR, Lee DW, Hinteregger GF: Roundscale spearfish Tetrapturus georgii: morphology, distribution, and relative abundance in the western north Atlantic. Bull Mar Sci 2008, 82:155-170.
• [13]Bernard AM, Shivji MS, Domingues RR, Viera Hazin FH, De Amorim AF, Domingo A, Arocha F, Prince ED, Hoolihan JP, Hilsdorf AWS: Broad geographic distribution of roundscale spearfish (Tetrapturus georgii) (Teleostei, Istiophoridae) in the Atlantic revealed by DNA analysis: implications for white marlin and roundscale spearfish management. Fish Res 2013, 139:93-97.
• [14]Schrope M: Fishy numbers for white marlin stocks. Proc Natl Acad Sci U S A 2013, 110:4151-4153.
• [15]Collette BB, McDowell JR, Graves JE: Phylogeny of recent billfishes (Xiphioidei). Bull Mar Sci 2006, 79:455-468.
• [16]Hanner R, Floyd R, Bernard A, Collette BB, Shivji M: DNA barcoding in billfishes. Mitochrondr DNA 2011, 22(Suppl 1):27-36.
• [17]Beerkircher LR, Serafy JE: Using head measurements to distinguish white marlin (Tetrapturus albidus) from roundscale spearfish (T. georgii). Bull Mar Sci 2011, 87:147-153.
• [18]Beerkircher LR, Arocha F, Barse A, Prince ED, Restrepo V, Serafy JE, Shivji MS: Effects of species misidentification on population assessment of overfished white marlin Tetrapturus albidus and roundscale spearfish T. georgii. Endanger Species Res 2009, 9:81-90.
• [19]WMBRT (White Marlin Billfish Review Team): Atlantic White Marlin Status Review. 2007.
• [20]Arocha F, Bárrios A: Sex ratios, spawning seasonality, sexual maturity, and fecundity of white marlin (Tetrapturus albidus) from the western central Atlantic. Fish Res 2009, 95:98-111.
• [21]Rocha LA: Patterns of distribution and processes of speciation in Brazilian reef fishes. J Biogeogr 2003, 30:1161-1171.
• [22]Rocha LA, Craig MT, Bowen BW: Phylogeography and the conservation of coral reef fishes. Coral Reefs 2007, 26:501-512.
• [23]Graves JE, McDowell JR: Genetic analysis of white marlin (Tetrapturus albidus) stock structure. Bull Mar Sci 2006, 79:469-482.
• [24]Alvarado Bremer JR, Mejuto J, Gómez-Márquez J, Boán F, Carpintero P, Rodríguez JM, Viñas J, Greig TW, Ely B: Hierarchical analyses of genetic variation of samples from breeding and feeding grounds confirms the genetic partitioning of northwest Atlantic and South Atlantic populations of swordfish (Xiphias gladius L.). J Exp Mar Biol Ecol 2005, 327:167-182.
• [25]Bernard AM, Feldheim KA, Shivji MS: Development and characterization of 11 novel microsatellite loci for the roundscale spearfish Tetrapturus georgii and their cross-species amplifcation among other istiophorid species. J Fish Biol 2012, 81:1781-1786.
• [26]Buonaccorsi VP, Graves JE: Isolation and characterization of novel polymorphic tetra-nucleotide microsatellite markers from the blue marlin, Makaira nigricans. Mol Ecol 2000, 9:817-829.
• [27]Schuelke M: An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 2000, 18:233-234.
• [28]Raymond M, Rousset F: GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 1995, 86:248-249.
• [29]Rousset F: Genepop '007: a complete reimplementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 2008, 8:103-106.
• [30]Guo SW, Thompson EA: Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 1992, 48:361-372.
• [31]Rousset F, Raymond M: Testing hertozygote excess and deficiency. Genetics 1995, 140:1413-1419.
• [32]Rice WR: Analyzing tables of statistical tests. Evolution 1989, 43:223-225.
• [33]El Mousadik A, Petit RJ: High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa (L.) Skeels) endemic to Morocco. Theor Appl Genet 1996, 92:832-839.
• [34]Goudet J: FSTAT, a program to estimate and test gene diversities and fixation indices v2.9.3 Release [http://www2.unil.ch/popgen/softwares/fstat.htm]
• [35]Chapuis M-P, Estoup A: Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 2007, 24:621-631.
• [36]Excoffier L, Laval G, Schneider S: Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinf Online 2005, 1:47-50.
• [37]Jost L: GSTand its relatives do not measure differentiation.Mol Ecol 2008, 17:4015–4026.
• [38]Chao A, Shen T-J: Program SPADE (Species Prediction And Diversity Estimation) [http://chao.stat.nthu.edu.tw/blog/software-download/spade/]
• [39]Hudson RR: A new statistic for detecting genetic differentiation. Genetics 2000, 155:2011-2014.
• [40]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
• [41]Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P: Calculations of population differentiation based on GSTand D: forget GSTbut not all of statistics.Mol Ecol 2010, 19:3845–3852.
• [42]R Development Core Team: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna; 2012.
• [43]Muths D, Grewe P, Jean C, Bourjea J: Genetic population structure of the Swordfish (Xiphias gladius) in the southwest Indian Ocean: Sex-biased differentiation, congruency between markers and its incidence in a way of stock assessment. Fish Res 2009, 97:263-269.
• [44]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
• [45]Falush D, Stephens M, Pritchard JK: Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics 2003, 164:1567-1587.
• [46]Hubisz MJ, Falush D, Stephens M, Pritchard JK: Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 2009, 9:1322-1332.
• [47]Guillot G, Mortier F, Estoup A: Geneland: a computer package for landscape genetics. Mol Ecol Notes 2005, 5:712-715.
• [48]Peakall R, Smouse PE: GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 2006, 6:288-295.
• [49]Guindon S, Gascuel O: A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 2003, 52:696-704.
• [50]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256.
• [51]Nei M: Molecular Evolutionary Genetics. Columbia University Press, New York; 1987.
• [52]Fu YX: Estimating the age of the common ancestor of a DNA sample using the number of segregating sites. Genetics 1996, 144:829-838.
• [53]Ramos-Onsins SE, Rozas J: Statistical properties of new neutrality tests against population growth. Mol Biol Evol 2002, 19:2092-2100.
• [54]Rogers AR, Harpending H: Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 1992, 9:552-569.
• [55]Harpending HC: Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 1994, 66:591-600.
• [56]Donaldson KA, Wilson RRJ: Amphi-Panamic germinates of snook (Percoidei: Centropomidae) provide a calibration of the divergence rate in the mitochondrial DNA control region of fishes. Mol Phylogenet Evol 1999, 13:208-213.
• [57]Sato A, Takezaki N, Tichy H, Figueroa F, Mayer WE, Klein J: Origin and speciation of haplochromine fishes in east African crater lakes investigated by the analysis of their mtDNA, Mhc genes, and SINEs. Mol Biol Evol 2003, 20:1448-1462.
• [58]Bowen BW, Muss A, Rocha LA, Grant WS: Shallow mtDNA coalescence in Atlantic pygmy angelfishes (Genus Centropyge) indicates a recent invasion from the Indian Ocean. J Hered 2006, 97:1-12.
• [59]Kuhner MK: Lamarc 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 2006, 22:768-770.
• [60]Kuhner MK: Coalescent genealogy samplers: windows into population history. Trends Ecol Evol 2009, 24:86-93.
• [61]Rambaut A, Drummond AJ: Tracer v1.5. [http://beast.bio.ed.ac.uk/Tracer]
• [62]Drummond AJ, Rambaut A: BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007, 7:214-222. BioMed Central Full Text
• [63]van Oosterhout C, Hutchinson WF, Wills DPM, Shipley PF: Micro-Checker User Guide v2.3 [http://www.microchecker.hull.ac.uk/]
• [64]Hasegawa M, Kishino K, Yano T: Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 1985, 22:160-174.
• [65]Ryman N, Palm S, André C, Carvalho GR, Dahlgren TG, Jorde PE, Laikre L, Larsson LC, Palmé A, Ruzzante DE: Power for detecting genetic divergence: differences between statistical methods and marker loci. Mol Ecol 2006, 15:2031-2045.
• [66]Waples RS, Gaggiotti O: What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 2006, 15:1419-1439.
• [67]Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OEJ: Relative performace of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conserv Genet 2006, 7:295-302.
• [68]Orozco-terWengel P, Corander J, Schlötterer C: Genealogical lineage sorting leads to significant, but incorrect Bayesian multilocus inference of population structure. Mol Ecol 2011, 20:1108-1121.
• [69]Balloux F, Lugon-Moulin N: The estimation of population differentiation with microsatellite markers. Mol Ecol 2002, 11:155-165.
• [70]Ryman N, Leimar O: GSTis still a useful measure of genetic differentation - a comment on Jost's D .Mol Ecol 2009, 18:2084–2087.
• [71]Buonaccorsi VP, Reece KS, Morgan LW, Graves JE: Geographic distribution of molecular variance within the blue marlin (Makaira nigricans): a hierarchical analysis of allozyme, single-copy nuclear DNA, and mitochondrial DNA markers. Evolution 1999, 53:568-579.
• [72]Buonaccorsi VP, McDowell JR, Graves JE: Reconciling patterns of inter-ocean molecular variance from four classes of molecular markers in blue marlin (Makaira nigricans). Mol Ecol 2001, 10:1179-1196.
• [73]Graves JE, McDowell JR: Stock structure of the world’s istiophorid billfishes: a genetic perspective. Mar Freshwater Res 2003, 54:287-298.
• [74]McDowell JR, Carlsson J, Graves JE: Genetic analysis of blue marlin (Makaira nigricans) stock structure in the Atlantic ocean. Gulf Caribb Res 2007, 19:75-82.
• [75]Dutton PH, Roden SE, Stewart KR, LaCasella E, Tiwari M, Formia A, Thomé JC, Livingstone SR, Eckert S, Chacon-Chaverri D, Rivalan P, Allman P: Population stock structure of leatherback turtles (Dermochelys coriacea) in the Atlantic revealed using mtDNA and microsatellite markers. Conserv Genet 2013, 14:625-636.
• [76]Moritz C: Defining ‘Evolutionary Significant Units’ for conservation. Trends Ecol Evol 1994, 9:373-375.
• [77]Die DJ: Are Atlantic marlins overfished or endangered? Some reasons why we may not be able to tell. Bull Mar Sci 2006, 79:529-544.
• [78]Carlsson J, McDowell JR, Díaz-Jaimes P, Carlsson JEL, Boles SB, Gold JR, Graves JE: Microsatellite and mitochondrial DNA analyses of Atlantic bluefin tuna (Thunnus thynnus thynnus) population structure in the Mediterranean Sea. Mol Ecol 2004, 13:3345-3356.
• [79]Alvarado Bremer JR, Viñas J, Mejuto J, Ely B, Pla C: Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes. Mol Phylogenet Evol 2005, 36:169-187.
• [80]Droxler AW, Alley RB, Howard WR, Poore RZ, Burckle LH: Unique and exceptionally long interglacial marine isotope stage 11: window into earth warm future climate. Geoph Monog Series 2003, 137:1-14.
• [81]McDowell JR, Graves JE: Population structure of striped marlin (Kajikia audax) in the Pacific Ocean based on analysis of microsatellite and mitochondrial DNA. Can J Fish Aquat Sci 2008, 65:1307-1320.
• [82]Purcell CM, Edmands S: Resolving the genetic structure of striped marlin, Kajikia audax, in the Pacific Ocean through spatial and temporal sampling of adult and immature fish. Can J Fish Aquat Sci 2011, 68:1861-1875.
• [83]Hoolihan J: ICCAT Manual Chapter 2.1.8.4. Roundscale Spearfish [http://www.iccat.int/Documents/SCRS/Manual/CH2/2_1_8_4_SPG_ENG.pdf]
• [84]Ho SYW, Shapiro B: Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol Ecol Resour 2011, 11:423-434.
• [85]Karl SA, Toonen RJ, Grant WS, Bowen BW: Common misconceptions in molecular ecology: echoes of the modern synthesis. Mol Ecol 2012, 21:4171-4189.
• [86]Arocha F, Silva J: Proportion of Tetrapturus georgii (SPG) with respect to T. albidus (WHM) in the Venezuelan pelagic longline catch in the western Caribbean Sea and adjacent Atlantic waters during 2002–2007. Coll Vol Sci Papers ICCAT 2011, 66:1787-1793.
• [87]Graves JE, McDowell JR: Inter-annual variability in the proportion of roundscale spearfish (Tetrapturus georgii) and and white marlin (Kajikia albida) in the western North Atlantic Ocean. Coll Vol Sci Papers ICCAT 2012, 68:1543-1547.