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Genetic Differentiation in the Antarctic Coastal Krill Euphausia Crystallorophias

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Genetic Differentiation in the Antarctic Coastal Krill Euphausia Crystallorophias Heredity (2002) 88, 280–287 2002 Nature Publishing Group All rights reserved 0018-067X/02 $25.00 www.nature.com/hdy Genetic differentiation in the Antarctic coastal krill Euphausia crystallorophias SN Jarman1,2,3, NG Elliott2, S Nicol3 and A McMinn1 1Institute of Antarctic and Southern Ocean Studies, University of Tasmania, GPO Box 252–77, Hobart, TAS, 7001, Australia; 2CSIRO Marine Research, GPO Box 1538, Hobart, TAS, 7001, Australia; 3Australian Antarctic Division, Channel Highway, Kingston, TAS, 7050, Australia The population genetics of the Antarctic neritic krill species ified. However, the extent of these differences did not corre- Euphausia crystallorophias was examined by nucleotide late with the degree of geographic separation between the sequence variation in its mitochondrial DNA. A 616 base pair sampling sites. This suggests that the genetic structuring region of the cytochrome c oxidase subunit I (COI) gene was may be the result of small-scale differentiation rather than screened for mutations by single-strand conformational poly- differentiation between resident populations in separate morphism (SSCP) combined with restriction digestion. E. parts of the Southern Ocean. The possibility that genetic dif- crystallorophias caught in three different regions of the Ant- ferences between samples within a region are as important arctic coastline were used – two samples from the Mertz as differences between regions has implications for other Glacier Polynya and one sample each from the western side studies of krill population genetics. of the Antarctic Peninsula and from the Davis Sea. Signifi- Heredity (2002) 88, 280–287. DOI: 10.1038/sj/hdy/6800041 cant genetic differences between krill samples were ident- Keywords: crustacea; genetics; krill; population; SSCP; swarm Introduction primary production and the macrofauna of the Antarc- tic coast. Krill (Malacostraca: Euphausiacea) are pelagic filter-feed- The population genetics of E. crystallorophias has been ing crustaceans. They are an abundant component of the investigated previously by Fevolden and Ayala (1981) pelagic ecosystem of all oceans. Most krill species have and by Ku¨hl and Schneppenheim (1985) using allozyme highly discontinuous distributions as a result of their electrophoresis. The first study compared allozyme fre- tendency to form dense swarms (Mauchline and Fisher, quencies in one sample of E. crystallorophias with fre- 1969). Krill play an important role in carbon and energy quencies for the same enzymes in several samples of transfer from the photosynthetic microorganisms on Euphausia superba, which is a close relative of E. crystallo- which they predominately feed to the diverse megafauna rophias (Patarnello et al, 1996; Jarman et al, 2000). The com- that prey on them (Mauchline and Fisher, 1969). parison in allele frequencies between the two species Euphausia crystallorophias Holt and Tattersall, 1906, demonstrated that there is negligible gene flow between commonly called ‘crystal krill’ or ‘Antarctic coastal krill’, them. Ku¨hl and Schenppenheim’s study examined allo- is the most southerly krill species. It inhabits the waters zyme frequency differences between four separate of the neritic zone between the Antarctic coast and the samples of E. crystallorophias and also made a comparison continental shelf to about 500 m depth (Mauchline and between these samples and samples of E. superba. For 17 Fisher, 1969). E. crystallorophias is the most abundant loci examined, no significant difference in allele euphausiid in these waters and is an important food frequency was found between two samples of E. crystallo- source for diverse coastal predators (Thomas and Green, rophias caught on the western side of the Antarctic Penin- 1988) including fish (La Mesa et al, 2000), whales (Ichii et sula and two samples taken from widely separated pos- al, 1998) and penguins (Ainley et al, 1998; Wienecke et itions in the Weddell Sea. A significant departure from al, 2000). It feeds on planktonic diatoms (Mauchline and genotype frequencies expected under Hardy-Weinberg Fisher, 1969), bacteria, detritus and other microorganisms equilibrium was recorded for only one of the enzymes, (Pakhamov and Perissinotto, 1996) as well as grazing the GPI. The authors concluded that E. crystallorophias forms algal communities that form on the underside of ice floes a single interbreeding population that is genetically dis- (Melnikov and Spiridinov, 1996). E. crystallorophias thus tinct and reproductively isolated from E. superba (Ku¨ hl forms probably the most important trophic link between and Schneppenheim, 1985). Several population genetic studies of krill in recent years have identified genetic differentiation within the Correspondence: S Jarman, CSIRO Marine Research, GPO Box 1538, subject species. Zane et al (1998) studied the population Hobart, TAS 7001, Australia. E-mail: Simon.JarmanȰmarine.csiro.au structure of E. superba with mitochondrial DNA sequen- Received 8 May 2001; accepted 16 November 2001 cing. Previous studies of this species with allozymes had Antarctic coastal krill genetics SN Jarman et al 281 found no significant genetic differentiation between Materials and methods widely separated samples (MacDonald et al, 1986; Fev- olden and Schneppenheim, 1989). The mitochondrial Sample collection DNA study found significant genetic structure in the Euphausia crystallorophias were collected from four ⌽ = species and significant pairwise Fst and st differences locations during 1999. A sample (n 61) was taken from between E. superba collected in the Wedell Sea and near the West Antarctic Peninsula region (66°53Ј S68°55Ј W) South Georgia, though not between any other pairwise in January 1999 during the austral summer. Two samples combinations of the four samples (Zane et al, 1998). Mito- (n = 59, 47) were collected from the Mertz Glacier Poly- chondrial DNA variation was also used by Bucklin et al nya (66°23Ј S 145°54Ј E; 66°29Ј S 146°1Ј E) in winter dur- (1997) and by Zane et al (1999) to examine the population ing September 1999. One sample (n = 65) was collected genetics of Meganyctiphanes norvegica. This species had from near the Shackelton Ice Shelf in the Davis Sea also previously been studied with allozymes, which did (65°32Ј S 107°0Ј E) during December 1999. Each sample not detect any population genetic structure (Sundt and is the result of a single, short (Ͻ10 min) net tow and is Fevolden, 1996), whereas the mitochondrial DNA studies assumed to be from one krill swarm or a small number of M. norvegica did identify population differentiation. In of adjacent aggregations. All samples were preserved in each case where genetic differentiation was identified the 75% ethanol until required for DNA extraction. authors suggested that the genetic differences between DNA isolation the samples were caused by restricted gene flow between A novel DNA purification method was used. About 50 different parts of each species’ range (Bucklin et al, 1997; mg of krill abdominal muscle was placed in a 1.5 ml et al Zane , 1998, 1999). microcentrifuge tube and homogenised in 400 ␮lof5M Biological variation between krill samples caught guanidine thiocyanate, 50 mM Tris pH 8.0, 0.5% Triton within one area has been demonstrated previously for the X-100 and 0.05% sodium dodecyl sulfate. This mixture Antarctic krill E. superba (Fevolden and George, 1984; was incubated on a shaking platform at 65°C for 2 h to Quentin and Ross, 1984; Watkins et al, 1986, 1990). For allow the chaotropic guanidine thiocyanate to denature example, significant differences were found in length, proteins (Bowtell, 1987; Chomczynski et al, 1997); and the weight, sex and maturity for krill caught in trawls at sodium dodecyl sulfate to disentangle them from DNA adjacent locations in the vicinity of South Georgia (Ausubel et al, 1997). Two hundred ␮l of 5 M NaCl was (Watkins et al, 1986, 1990). This observation was pursued added to precipitate proteins (Miller et al, 1988), which further by Watkins et al (1990) who found the minimum were pelleted by centrifugation at 20 000 g for 20 min. number of krill samples needed to get a reliable estimate The resulting supernatant was poured into a new tube of krill population parameters in a geographic area such containing 200 ␮l 0.5 ␮g/␮l proteinase K. The solutions as the ocean around South Georgia. For all population were mixed and incubated on a shaking platform at 65°C parameters assessed, more than 14 samples of 100 indi- for 2 h. Five hundred ␮l 100% ethanol was added to pre- viduals are needed to get an unbiased estimate. Temporal cipitate nucleic acids, which were pelleted by centrifug- variation in population parameters for E. superba has also ation at 20 000 g for 20 min. Most of the contaminating been demonstrated by Reid et al (1999) who found sig- polysaccharides were held in solution at this stage by the nificant inter-annual variation in mean length of krill in Ͼ1 M NaCl concentration (Fang et al, 1992) and discarded this same region. These studies demonstrate that single with the supernatant. The precipitated pellet of DNA was samples of krill from one area do not provide a reliable washed in 70% ethanol to remove residual salts, air dried estimate of the population characteristics of krill in that and then dissolved in 100 ␮l 10 mM Tris pH 8.0. area. The assumption of previous population genetic studies of krill, that single hauls of krill can adequately Amplification of mitochondrial DNA describe genetic population parameters for a region in A 616 base pair region of the mitochondrial COI region was amplified with the polymerase chain reaction (PCR) space and time, may therefore also be incorrect. Ј In this study the population genetics of E. crystalloro- using ‘universal’ primer HCO (5 -taaacttcagggtgac- caaaaaatca-3Ј) (Folmer et al, 1994) and the species-specific phias is studied with the frequency of mitochondrial DNA Ј Ј haplotypes in different krill samples. DNA sequence vari- primer EcLCO (5 -ggtgcgtgagctgggatagtggg-3 ). EcLCO ation in the 5Ј end of the mitochondrial cytochrome c oxi- was designed on the sequence previously reported for a dase subunit I (COI) gene was identified using the single slightly longer segment of the E.
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