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Multiple Genetic Stocks of Longfin Squid Loligo Pealeii in the NW Atlantic: Stocks Segregate Inshore in Summer, but Aggregate Offshore in Winter

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Multiple Genetic Stocks of Longfin Squid Loligo Pealeii in the NW Atlantic: Stocks Segregate Inshore in Summer, but Aggregate Offshore in Winter MARINE ECOLOGY PROGRESS SERIES Vol. 310: 263–270, 2006 Published April 3 Mar Ecol Prog Ser Multiple genetic stocks of longfin squid Loligo pealeii in the NW Atlantic: stocks segregate inshore in summer, but aggregate offshore in winter K. C. Buresch, G. Gerlach, R. T. Hanlon* Marine Resources Center, Marine Biological Laboratory, Woods Hole, Massachusetts 02543, USA ABSTRACT: The longfin squid Loligo pealeii is distributed widely in the NW Atlantic and is the tar- get of a major fishery. A previous electrophoretic study of L. pealeii was unable to prove genetic dif- ferentiation, and the fishery has been managed as a single unit stock. We tested for population struc- ture using 5 microsatellite loci. In early summer (June), when the squids had migrated inshore to spawn, we distinguished 4 genetically distinct stocks between Delaware and Cape Cod (ca. 490 km); a 5th genetic stock occurred in Nova Scotia and a 6th in the northern Gulf of Mexico. One of the sum- mer inshore stocks did not show genetic differentiation from 2 of the winter offshore populations. We suggest that squids from summer locations overwinter in offshore canyons and that winter offshore fishing may affect multiple stocks of the inshore fishery. In spring, squids may segregate by genetic stock as they undertake their inshore migration, indicating an underlying mechanism of subpopula- tion recognition. KEY WORDS: Fisheries · Spawning migration · Microsatellites · Population structure · Population recognition · Null alleles Resale or republication not permitted without written consent of the publisher INTRODUCTION Most loliginid fisheries, including that for the longfin squid Loligo pealeii (Lesueur 1821), are managed as a The high dispersal capability of many marine organ- single unit stock (NEFSC 1996). The reason for this is isms has typically been associated with low levels of that most studies of genetic structuring in squid popula- genetic differentiation, especially when compared to tions have suggested widespread genetic uniformity terrestrial and freshwater species (Ward et al. 1994, (e.g. Garthwaite et al. 1989, Reichow & Smith 2001, Graves 1998, Waples 1998). Several recent studies Shaw et al. 1999, 2004). In addition, offshore of the At- using highly variable genetic markers have shown lantic coast of the USA, the lack of conspicuous physical examples of marine organisms that do exhibit popula- oceanographic barriers to gene flow would suggest that tion substructure (for reviews see Bohonak 1999, Hell- separate genetic stocks are unlikely to exist. berg et al. 2002). The presence of distinct genetic units Loligo pealeii has a life span <1 yr, due in large part within commercially important species bears direct to the very high growth rates that squids achieve (Hat- relevance to the management of fisheries. field et al. 2001), and to the relatively small sizes at Population genetic structure of cephalopods is scarcely which the species is capable of maturing under certain known. Within the Class Cephalopoda (Phylum Mol- (yet unknown) conditions. Off southern New England lusca), the squids (Order Teuthoidea) are one of the most (the main fishery), squids are found inshore in summer speciose and numerically abundant groups, and play a as they spawn, and offshore during winter in subma- central role in marine ecosystems (cf. Boyle & Boletzky rine canyons with stable temperatures (Summers 1996). Among the world’s inshore fisheries, the loliginid 1983). There is evidence that they also undergo sub- squids (Family Loliginidae) are now one of the most com- stantial north-south migrations on the order of 500 km mercially valuable species. These stocks must be man- or more (Macy & Brodziak 2001). Recent morphometric aged judiciously due to recent high levels of exploitation. studies of size and age at maturity provide evidence *Corresponding author. Email: [email protected] © Inter-Research 2006 · www.int-res.com 264 Mar Ecol Prog Ser 310: 263–270, 2006 that the link between inshore and offshore compo- PCR products were separated on a 6% denaturing poly- nents of the stock may be more complicated than for- acrylamide gel, and analyzed on a LI-COR 4000 model merly believed: age structure remains nearly constant sequencer. Fragment sizes were determined by com- through winter and spring, and statolith back-aging parison to commercial size standards (LI-COR) using suggests that spawning recruitment may occur year- GelPro Analyzer software (Media Cybernetics). Samples round (Macy & Brodziak 2001). of alleles of known size were run on each gel as stan- An allozyme study of Loligo pealeii showed that only 1 dards to assure correct allele assignment. Allele lengths locus was polymorphic enough to detect differentiation that could not be determined the first time were repeat- (Garthwaite et al. 1989). Based upon that single locus, edly run until unequivocal assignment. those authors suggested that 3 separate populations of L. pealeii existed along the Atlantic coast of the USA at Virginia, Cape Cod, and Georges Bank. However, the L. pealeii fishery has continued to be managed as a sin- gle genetic stock, given the lack of convincing genetic data to the contrary. Because recent increases in value have attracted attention to the L. pealeii fishery, and due to refinement of molecular genetic techniques, we de- cided to use microsatellites (Buresch et al. 2001, Maxwell et al. 2000) to test for population substructure. MATERIALS AND METHODS Sample collection. Squid samples were collected by trawl from 6 inshore areas: Nova Scotia (Stn 1), Cape Cod (Stn 2), Long Island Sound (Stn 3), New Jersey (Stn 4), Delaware (Stn 5), and northern Gulf of Mexico (Stn 6); 1 mid-shelf area: Georges Bank (Stn 7); and 3 off- shore areas: Veatch Canyon (Stn 8), Hudson Canyon (Stn 9), and Washington Canyon (Stn 10) (Fig. 1). In- shore summer samples and the mid-shelf sample were collected during the 2001 spawning season from May to June. Winter offshore samples were collected from dif- ferent years (Table 1). The northern Gulf of Mexico (Stn 6), Hudson Canyon (Stn 9), and Nova Scotia (Stn 1) samples were collected during winter 2000, prior to the inshore summer sampling. Washington (Stn 10) and Veatch (Stn 8) canyons were sampled in winter 2002, after the inshore summer samples. DNA extraction, amplification and genotyping. Squids were frozen until DNA extraction. Genomic DNA was extracted from 20 to 40 mg of adult arm tip tissue by a variation of the phenol/SDS procedure (Sambrook et al. 1989). Five microsatellite primers (Lfor3, Lp2, Lp4, Lp5 and Lp12) (Maxwell et al. 2000) were applied to each sample. Microsatellites were amplified using the polymerase chain reaction (PCR) in a Perkin Elmer 3700 thermocycler under the following conditions: 300 s at 95°C, then 25 to 35 cycles of 30 s at 95°C, 30 s at 55°C, 30 s at 72°C, and a final elongation time of 120 s. Re- action mixes contained 1 µl of template DNA, 1.5 mM Fig. 1. Loligo pealeii. Sampling stations in the NW Atlantic. (a) In- MgCl2, 0.2 mM of each nucleotide, 0.1 mM of each shore–offshore connections; (b) offshore connections only. Rectan- primer (1 primer infrared labeled), 0.08 units of Taq poly- gles: summer samples; circles: winter samples. Connecting lines: non-significant differences in allele frequencies (i.e. gene flow) merase (Promega) with the manufacturer’s supplied between stocks; dotted line: non-significant FST value; inset: Gulf of Buffer B, and deionized water to a final volume of 10 µl. Mexico sampling station Buresch et al: Multiple genetic stocks of longfin squid 265 Table 1. Loligo pealeii. Sampling stations and collection details (compare with is, if the smallest allele was 103, we Fig. 1). In: inshore; Mid: mid-shelf; Off: offshore. W: winter; S: summer named the (probably) falsely assigned second allele ‘100’ because we used trin- Sampling ucleotide repeat loci. This introduced a Stn Name Latitude Longitude Size Location Period conservative bias because null alleles 01 Nova Scotia 44.0° N 66.8° W 45 In W 2001–2002 may consist of several size classes them- 02 Cape Cod 42.0° N 70.2° W 38 In S 2001 selves, in which size-homoplasy tends to 03 Long Island 41.2° N 72.5° W 93 In S 2001 reduce the ‘true’ population divergence. 04 New Jersey 39.4° N 74.3° W 76 In S 2001 We used these corrected alleles for cal- 05 Delaware 38.6° N 75.0° W 61 In S 2001 06 Gulf of Mexico 29.3° N 94.8° W 45 In W 2000–2001 culating genetic divergence among pop- 07 Georges Bank 41.5° N 68.5° W 42 Mid S 2001 ulations (FST values) and for the Mantel 08 Veatch Canyon 40.2° N 69.6° W 34 Off W 2001–2002 test. Since RST values are calculated us- 09 Hudson Canyon 39.5° N 72.0° W 30 Off W 2000–2001 ing similar alleles, they cannot be calcu- 10 Washington Canyon 37.4° N 74.5° W 20 Off W 2001–2002 lated after correcting for null alleles. Data analysis. Observed and expected heterozygo- sities were calculated for each locus, and genotypes RESULTS were tested for linkage disequilibrium to determine in- dependence of loci using FSTAT version 2.93 updated All 5 microsatellite loci were highly polymorphic, from Goudet (1995). Genotype and allele frequencies of ranging from 15 to 37 different alleles per locus; loci the microsatellite loci were used to estimate variances in Lp2 and Lp4 exhibited the greatest number of alleles gene frequencies within and among sampling stations. (Table 2). No significant linkage disequilibrium was Within subpopulations, deviations from Hardy-Wein- found among loci. Observed levels of heterozygosity berg equilibrium were estimated by FIS values calculated ranged from 66 to 88%.
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