Mar Biodiv (2018) 48:1027–1035 DOI 10.1007/s12526-017-0774-4 ORIGINAL PAPER Postglacial expansion of the Arctic keystone copepod Calanus glacialis 1,2 1 1 Agata Weydmann & Aleksandra Przyłucka & Marek Lubośny & 2 3 3 1 Katarzyna S. Walczyńska & Ester A. Serrão & Gareth A. Pearson & Artur Burzyński Received: 22 February 2016 /Revised: 10 July 2017 /Accepted: 27 July 2017 /Published online: 15 August 2017 The Author(s) 2017. This article is an open access publication Abstract Calanus glacialis, a major contributor to zooplank- Introduction ton biomass in the Arctic shelf seas, is a key link between primary production and higher trophic levels that may be sen- A large part of zooplankton biomass in the Arctic shelf seas is sitive to climate warming. The aim of this study was to explore formed by Calanus glacialis (Fleminger and Hulseman, 1977; genetic variation in contemporary populations of this species Blachowiak-Samolyk et al. 2008; Weydmann et al. 2013), a to infer possible changes during the Quaternary period, and to lipid-rich calanoid grazer. In the lipid-based Arctic food web, assess its population structure in both space and time. Calanus it is an essential link between the low-energy microalgae and glacialis was sampled in the fjords of Spitsbergen (Hornsund higher trophic levels (Lee and Hirota 1973; Falk-Petersen and Kongsfjorden) in 2003, 2004, 2006, 2009 and 2012. The et al. 2009). Its life cycle is between one (MacLellan 1967; sequence of a mitochondrial marker, belonging to the ND5 Weydmann et al. 2013) and three years (Kosobokova 1999), gene, selected for the study was 1249 base pairs long and depending on the region and environmental conditions, al- distinguished 75 unique haplotypes among 140 individuals though C. glacialis typically has a 2-year life span (Hirche that formed three main clades. There was no detectable pattern and Kwaśniewski 1997). The areas of its occurrence, includ- in the distribution of haplotypes by geographic distance or ing peripheral seas of the Arctic Ocean and adjacent regions of over time. Interestingly, a Bayesian skyline plot suggested that the North Atlantic and Pacific Oceans (Jashnov 1970; a 1000-fold increase in population size occurred approximate- Conover 1988), are now facing intensive modifications from ly 10,000 years before present, suggesting a species expansion an unprecedented combination of environmental changes, after the Last Glacial Maximum. such as increasing ocean temperatures and reduction in sea ice extent, caused by climate warming (IPCC 2014), with the record high Atlantic Water temperature and salinity in . . . Keywords Calanus Zooplankton mtDNA Population 2006 (Walczowski et al. 2012). With the Arctic region likely genetics Genetic diversity to continue warming more rapidly than the global mean (IPCC 2014), changes are expected to affect Arctic marine biota. For example, the loss of sea ice represents a loss of critical habitat Communicated by R. R. Hopcroft for ice-related species, such as C. glacialis, that needs energy from the ice algal bloom to fuel its reproduction (Søreide et al. * Agata Weydmann 2010). Major changes in the function of the Arctic marine firstname.lastname@example.org ecosystem are now anticipated. The capacity for populations to evolve in response to envi- ronmental changes is based on genetic diversity, which en- Institute of Oceanology, Polish Academy of Sciences, Powstańców Warszawy 55, 81-712 Sopot, Poland compasses the variation among individuals within a popula- tion and the genetic variation among populations (Gray 1997; Institute of Oceanography, University of Gdańsk, al. Marszałka Piłsudskiego 46, 81–378 Gdynia, Poland Kenchington et al. 2003; Reed and Frankham 2003). Climatic changes during the Quaternary period in Arctic regions, with CCMAR, University of Algarve, Campus de Gambelas, 8005-139 Faro, Portugal repeated glacial and interglacial periods causing cyclical 1028 Mar Biodiv (2018) 48:1027–1035 expansions and contractions of species, have shaped their ge- Material and methods netic variation and genealogies. During this time, some pop- ulations and lineages became extinct, while others underwent Study area bottlenecks and founder events. Mitochondrial markers, which provide suitably variable sequences, are among the Our study area covered two fjords in the Atlantic sector of the most favored for tracking such events during the Quaternary Arctic Ocean. Hornsund is a medium-sized fjord located in the (Hewitt 2004). southwest part of Spitsbergen (Fig. 1). The fjord is under the To adequately assess patterns of genetic diversity at the influence of the cold coastal South Cape Current and warmer, population level, fast-evolving markers should be used, par- more saline West Spitsbergen Current. The inner fjord basin, ticularly for the study of animal populations that have expand- Brepollen, is isolated from the main basin by an underwater ed substantially since the Last Glacial Maximum 10,000– sill establishing a reservoir of winter cooled water throughout 14,000 years ago (Baker 2000). To date, few Arctic species all seasons (Swerpel 1985), where a local population of have been studied in detail. The lack of adequate polymorphic C. glacialis was reported to exist (Weydmann and makers was one of the factors limiting genetic research in Kwaśniewski 2008). Calanus spp., although several microsatellite markers have Kongsfjorden is an open fjord situated on the west coast of recently been published (Provan et al. 2007; Provan et al. Spitsbergen. Due to the absence of a sill at the entrance, the 2009;Parentetal. 2012; Weydmann et al. 2014). Provan fjord faces strong pulsed influxes of relatively warm Atlantic et al. (2009) used microsatellite markers and mitochondrial water (Cottier et al. 2005). Despite the fjord’slocation at 79°N cytochrome b gene (CYTB)in Calanus finmarchicus,reveal- latitude, the fauna of Kongsfjorden is of a rather sub-arctic ing no significant genetic differentiation at the inter- character due to the strong influence of the West Spitsbergen population level or across the species’ range, in either nuclear Current and advection processes (Kwaśniewski et al. 2003; or mitochondrial data sets. The authors postulated that these Walkusz et al. 2009). results indicated high levels of dispersal and a constant effec- tive population size over the period 359,000–566,000 years Sampling before present, and suggested that C. finmarchicus possessed the capacity to track changes in available habitat, a feature that Zooplankton samples were collected from the fjords during may be of crucial importance for the species’ ability to cope the summers of 2003 (Hornsund), 2004 (Kongsfjorden), 2006 with the current period of global climate change. However, (Hornsund), 2009 (Kongsfjorden), and 2012 (both fjords) similar studies have not been conducted on its Arctic sibling, (Table 1) during the Arctic cruises of the R/V Oceania,using C. glacialis. Using the 16S ribosomal RNA gene, Nelson et al. a WP-2 mesozooplankton net (0.25 m mouth opening; (2009) defined two genetically distinct C. glacialis popula- 180 μm mesh size), and were preserved in 96% ethanol, tions—an Arctic and a North Pacific (Bering Sea) popula- which was changed 24 h after sampling. tion—although the latter was not reproductively established in the Arctic Ocean. The authors suggested that climate DNA extraction and amplification warming could increase opportunities for southern organisms to become established in the Arctic. In contrast, Weydmann In total, 140 Calanus glacialis individuals of the fifth et al. (2016), on the basis of microsatellite markers, reported a copepodite stage and adult females were identified to the spe- panmictic population of C. glacialis with large-scale gene cies level based on the prosome length (Weydmann and flow around the Arctic. Kwasniewski 2008) and characteristic morphological features Here we aimed to estimate genetic variation in contempo- (Brodskii et al. 1983) and were retrieved from the mixed zoo- rary populations of Calanus glacialis to examine possible plankton samples. Their genomic DNA was extracted using changes during the Quaternary, especially after the Last the Sherlock AX kit (A&A Biotechnology). Glacial Maximum, when major latitudinal species range shifts Specific PCR primers (popF: 5’-AAGATACTTGGTAT occurred. Additionally, we wished to assess the recent popu- ATTTCTGACACC-3’, popR: 5’-ATATTTATGTTGAT lation structure of this key Arctic zooplankton species at both TCTCAGCCC-3’) and a third sequencing primer (popR2 5’- geographic and temporal scales. To this end, we chose two TTCACAATATAAAAGATTACC-3’) were designed using Spitsbergen fjords (Svalbard Archipelago) that are contrasting sequences available in the NCBI database of sequence read in terms of water masses, in addition to the availability of archives (SRA, accession numbers SRR1793125, samples from a time series collected between 2003 and SRR1791606, SRR1791605, SRR1791524, SRR1791525) 2012. Finally, we based our study on a newly developed mi- (Ramos et al. 2015). The PCR product, covering 1465 base tochondrial marker, chosen based on the length of mitochon- pairs (bp) of the mitochondrial ND5 gene encoding the fifth drial genes, and intermediate intra- and interspecies polymor- subunit of the respiratory chain complex I (NADH dehydro- phism, which is greater than those used to date. genase subunit 5), was obtained. This fragment was chosen Mar Biodiv (2018) 48:1027–1035 1029 Fig. 1 The Svalbard Archipelago with a schematic circulation of the dominant ocean currents and locations of sampling stations based on the length of mitochondrial genes, their intermediate PCR amplification protocol was as follows: initial denatur- intra- and interspecies polymorphism in comparison to con- ation at 95°C for 5 min, followed by 30 cycles of denaturation served CYTB, cytochrome oxidase subunit I (COI) and highly at 94°C for 30 s, annealing at 56°C for 30 s, and extension at variable NADH dehydrogenase subunits 3 and 4 (ND3 and 72°C for 2 min. The final extension lasted 5 min ND4) genes in the copepod subclass (Minxiao et al. 2011). (TProfessional Gradient Cycler from Biometra). The final reaction volume for PCR amplification was 10 μl, PCR products were separated by a 1% agarose gel electro- with approximately 5 ng of total DNA, 0.5 μMof popF and phoresis in 0.5X TBE buffer and visualized with ethidium popR primers, dNTPs at 200 μMeach, 2mM MgCl and 0.5 bromide in UV light. Products which showed a strong band U of DyNAzyme EXT DNA Polymerase (Thermo Fisher of the correct size were selected for sequencing. DNA con- Scientific), in a buffer supplied by the manufacturer. The centration was estimated based on gel images, and the Table 1 Sampling details: Fjord Sample Latitude Longitude Date Sampling depths Number of stations' positions, sampling (°N) (°E) (m) individuals depths, dates and the number of Calanus glacialis individuals Kongsfjorden K2004 78° 53.35 12° 27.62 22.07.2004 0–70 17 sequenced K2009 78° 57.03 11° 50.16 01.08.2009 0–60 16 K2012 78° 53.21 12° 27.43 07.08.2012 0–70 25 Hornsund H2003 76° 58.63 15° 45.66 25.07.2003 85–140 31 H2006 77° 00.47 16° 28.46 22.07.2006 50–120 21 H2012 77° 00.54 16° 28.30 01.08.2012 30–100 30 1030 Mar Biodiv (2018) 48:1027–1035 products were cleaned using Exonuclease I and alkaline phos- Results phatase treatment (Werle et al. 1994). Sequencing was per- formed by Sanger technology, in both directions, using all A 1249-bp long fragment of mitochondrial DNA, encoding part three primers (Macrogen, Inc.). of the ND5 gene, was sequenced in six samples of C. glacialis (Table 1). The diversity indices showed overall high haplotype Bioinformatic analysis diversity (Hd), which was apparently associated with low nucle- otide diversity (π) in the studied population of C. glacialis The raw sequence reads were assembled using Staden (Table 2). There were 75 haplotypes among 140 sequenced Package software (Staden 1996). The resulting partial ND5 individuals (Hd = 0.892). Despite this appreciable number of sequences were aligned in MEGA6 (Tamura et al. 2013)using haplotypes, the overall nucleotide diversity was very low, at the the ClustalW (Larkin et al. 2007) algorithm and trimmed to level of π = 0.004. There was no genetic differentiation between the same length of 1249 base pairs. The alignment was tested pairs of populations (population pairwise Φ did not ST straightforward, as there were no indels in the sequences. All differ significantly from zero); hence there was no evidence of sequences were deposited in GenBank under accession num- any population genetic structure among the compared samples bers MF447532 - MF447671. (p > 0.05; Table 3). Various groupings were checked for possible General diversity indices were calculated in DnaSP higher-level structuring using AMOVA, but no significant fixa- (Librado and Rozas 2009): haplotype diversity (Hd), tion indices were recovered, regardless of the grouping tested which is expected to be high for organisms with large (data not shown). The MSN of all haplotypes (Fig. 2)wasrel- effective population sizes (Hd close to 1); nucleotide di- atively simple and well-resolved, with three closely related hap- versity (π), which is expected to be within 1% for intra- lotypes surrounded by several minor-frequency variants. species mitochondrial polymorphism; and Tajima’s D sta- However, there was no visible trend in the distribution of hap- tistics used to test the departure of haplotype distribution lotypes by geographic location (Fig. 2a) or year of sampling from neutral expectations. To check for genetic differenti- (Fig. 2b). Taking into account the lack of structuring, all subse- ation among samples, analysis of molecular variance quent analyses were run on a combined set of all 140 sequences (AMOVA), including population pairwise fixation indices obtained. (Φ , with no. of permutations for significance = 1000) Tajima’s D test statistic was significantly negative (D = ST wascalculatedinArlequin3.5 (Excoffier andLischer −2.51, p < 0.05), indicating an excess of rare variants and 2010). A minimum spanning network (MSN) of all ob- hinting at possible recent population expansion. To test this served haplotypes was built using a median-joining algo- interpretation and to elucidate the demographic history of the rithm (Bandelt et al. 1999) implemented in Network soft- studied population of C. glacialis, BSP analysis was per- ware (fluxus-engineering.com). This type of analysis is formed (Fig. 3). The resulting plot indicates a strong increase more appropriate for population-level data than classic in population size occurring at approximately the time suffi- −4 −4 phylogenetic tree building, and allows quick visual inspec- cient to accumulate between 6×10 and 9×10 substitutions −4 tion of existing relationships between genetic diversity and per site, with a relatively wide CI of 4×10 substitutions. other factors (such as geographic or temporal scales). To Facing the complete lack of possible calibration points, the elucidate the demographic history of the studied popula- dating of this event can only be highly provisional. However, tion of C. glacialis, analysis of population size changes in order to fall within the postglacial limit, the expansion start −4 was performed in BEAST 2.4.5 (Bouckaert et al. 2014) (9×10 substitutions) would have to be inferred at no more using a Bayesian skyline plot (BSP) reconstruction ap- than 2×10 years before present (the Last Glacial Maximum). proach. The best-fit model of substitutions (HKY+G) as Accordingly, to fit our data within the confidence limits, the well as clock model (relaxed uncorrelated lognormal substitution rate would have to be in the range of 3.5–5.5% per −4 −4 4 clock) was selected using Bayes factor comparison MY ([9×10 − 2×10 ]/2×10 substitutions per site per year (Baele et al. 2012). No constrains were used; therefore, for the lower limit). Assuming a lower substitution rate would the obtained plots were scaled in mutational units. The push the expansion event out of the interglacial. Markov chain Monte Carlo (MCMC) was run for 10 mil- lion generations, in four replicates. The default 25% of initial (burn-in) generations was discarded after inspection Discussion of the results in Tracer v1.6 (Rambaut et al. 2014). All runs converged at the same solution; hence the resulting Our study revealed no evidence of genetic structure in log and tree files were combined. The effective sample Calanus glacialis among the fjords compared nor among size (ESS) of all parameters exceeded 300, ensuring that different years of sampling, regardless of their classification the results of the analysis were meaningful. BSP was cre- as warm (2006) or cold (2003, 2004). The results are ated in Tracer using combined tree and log files. similar to those by Weydmann et al. (2016), who reported a Mar Biodiv (2018) 48:1027–1035 1031 Table 2 Standard diversity Fjord Sample n Hd sd π sd π π D p indices for the sampled s a population of C. glacialis K2004 12 0.934 0.046 0.0039 0.00033 0.01397 0.00063 −0.99000 >0.1 K2009 13 0.950 0.048 0.0040 0.00063 0.01426 0.00066 −1.12811 >0.1 K2012 13 0.807 0.079 0.0037 0.00039 0.01305 0.00060 −1.19952 >0.1 H2003 21 0.916 0.043 0.0037 0.00052 0.01165 0.00062 −1.99554 <0.05 H2006 16 0.929 0.051 0.0064 0.00134 0.01564 0.00256 −1.73006 >0.05 H2012 19 0.871 0.060 0.0033 0.00045 0.01148 0.00064 −1.57126 >0.1 All 75 0.892 0.024 0.0040 0.00031 0.01298 0.00092 −2.50683 <0.001 Number of unique haplotypes (n), haplotype diversity (Hd), nucleotide diversity (π) along with the estimate of its standard deviation (sd), nucleotide diversity at synonymous (π ) and non-synonymous (π ) sites as well as the s a results of Taijima’s D test (D and p) calculated in DnaSP are shown. The last row (All) represents the indices calculated for the combined data set comprising all 140 sequences lack of genetic structure in C. glacialis from seven locations clades represented by them (Network software documentation, distributed around the Arctic (Svalbard fjords, White Sea, and www.fluxus-engineering.com). Recent population expansions Amundsen Gulf), sampled in 2008 and 2009, in support of the are also known to leave certain traces in the observed diversity hypothesis that large-scale effective dispersal and gene flow indices. The excess of rare polymorphism is expected in such driven by ocean currents allows for the free exchange of situations, leading to significantly negative Tajima’s D test planktonic copepods in the Arctic. Therefore, we believe the statistic (Tajima 1989), which was the case in our study. results would be similar even if we had sampled more sites This excess can also be caused by selection acting on the around the Arctic. There is also numerous evidence of pan- studied marker; however, in the case of a mitochondrial mark- mictic populations and/or high gene flow of planktonic cope- er it is usually assumed that demographic processes are re- pods across extensive geographic ranges of the Northern sponsible for this phenomenon (Grant 2015). Hemisphere, which has been reported for the Atlantic Multilocus data are known to be better for inferring demo- Calanus finmarchicus (Provan et al. 2009), Pacific Calanus graphic histories, particularly when combined with ancient sinicus (Huang et al. 2014), cosmopolitan Clausocalanus DNA sampling (Grant 2015). Unfortunately, for various tech- arcuicornis (Blanco-Bercial et al. 2011), and Arctic nical reasons, such data are currently unavailable for Calanus Pseudocalanus minutus (Aarbakke et al. 2014; Questel et al. species. Active marker development is ongoing (Smolina 2016). At the same time, to our knowledge, there is only one et al. 2014; Weydmann et al. 2014), but is hampered by the study confirming the existence of two populations of atypical genome organization in Calanus. Also, using a single C. glacialis, in the Arctic and the North Pacific (Bering mitochondrial gene has some advantages: as a maternally Sea), although the latter was not reproductively established inherited, haploid genome, it has a smaller effective popula- in the Arctic Ocean (Nelson et al. 2009). tion size and is more prone to bottleneck effects (Hartl and Although there was no connection to locations or time in Clark 2007). Therefore, the expansion seen in our data was not the distribution of C. glacialis haplotypes, one interesting fea- necessarily preceded by a very strong bottleneck. ture of the observed topology was the existence of star-like The rapid change recorded on the BSP plot (Fig. 3) confirms elements in the MSN: single, dominant haplotypes connected that the studied population had undergone an expansion. The by short branches with several low-frequency haplotypes (Fig. observed high haplotype diversity is indicative of a large effec- 2). Such structures usually indicate recent expansion of the tive population size, typically expected for a planktonic marine invertebrate. The causes of the observed pattern can be attrib- uted to the bottleneck experienced by C. glacialis during the Table 3 Genetic differentiation between pairs of samples. Above diagonal: pairwise p-values; below diagonal: fixation indices (Φ ) Pleistocene glaciation and the following rapid expansion of this ST species after the Last Glacial Maximum, when the Arctic was H2003 K2004 H2006 K2009 H2012 K2012 exposed to warming, resulting in a transition from full glacial conditions to widespread interglacial conditions attained ap- H2003 0.324 0.153 0.919 0.982 0.207 proximately 10,000 years ago. Such expansion is common K2004 −0.001 0.595 0.622 0.297 0.892 for many Arctic species, which survived in a few refugia and H2006 0.018 −0.007 0.279 0.189 0.315 very rapidly recolonized their current ranges after deglaciation; K2009 −0.022 −0.021 0.005 0.856 0.559 their current genetic diversity depends largely on the number of H2012 −0.020 −0.004 0.016 −0.024 0.270 refugia and effective population sizes of the surviving popula- K2012 0.015 −0.029 0.011 −0.017 0.006 tions (Hewitt 2000;Hewitt 2004 ). Marine species like 1032 Mar Biodiv (2018) 48:1027–1035 Fig. 2 The minimum spanning networks (MSN) of ND5 haplotypes of Calanus glacialis from the fjords of Spitsbergen. Circle diameters are proportional to the number of individuals bearing each haplotype, and lines connecting circles are roughly proportional to the number of mutational steps connecting haplotypes. a Distribution of haplotypes between sampling locations; number of individuals is also shown here. b Distribution of haplotypes between sampling years; exact numbers of mutational steps are shown here C. glacialis are additionally affected by ocean currents that with the most conservative COX1 gene, while the ND5 se- contribute to mixing processes between their populations. quence is most likely evolving much faster. Recent The question remains whether this explanation is plausible mitogenomic analysis of Metacrangonyctidae crustaceans and the estimated substitution rates are acceptable. The typi- (Pons et al. 2014) have shown that ND5 is among the cally assumed general mitochondrial substitution rates are fastest-evolving mitochondrial genes and accumulates substi- based on separating pairs of shrimp species by the emerging tutions about twice as fast as COX1. Isthmus of Panama (Knowlton et al. 1993; Knowlton and Direct estimates of the substitution rate are rare, but Haag- Weigt 1998) and a relatively short fragment of the conserved Liautard et al. (2008) measured the mitochondrial mutation −8 COX1 gene. It is assumed that other crustaceans, including rate in Drosophila. The obtained value of 6.2 × 10 per site −8 Calanus species, accumulate mitochondrial substitutions at a per fly generation would correspond to 3.1 × 10 per site per similar pace, resulting in the 1.4–2.2% increase in overall year for C. glacialis (assuming the 2-year generation time). divergence per million years (Papadopoulos et al. 2005). That would fit our requirement reasonably well, further indi- The substitution rate needed to attribute the observed expan- cating that the assumed substitution rate is quite plausible. sion in C. glacialis to the last interglacial is 3.5% per million Another important consideration is the apparent time de- years, leading to the accumulation of divergence at the speed pendency of molecular rate estimates (Ho et al. 2005), fre- of at least 7% per million years, a value seemingly much quently leading to large errors in calibrating recent events by higher but still in the same order of magnitude. At least two using rate estimates derived from phylogenetic species sepa- factors must be considered, each acting in favor of the in- rations (Grant 2015). These effects are difficult to mea- creased substitution rate. First, the published data are dealing sure, but they both act in the same direction: towards the Mar Biodiv (2018) 48:1027–1035 1033 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http:// creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appro- priate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. References Aarbakke ONS, Bucklin A, Halsband C, Norrbin F (2014) Comparative phylogeography and demographic history of five sibling species of Pseudocalanus (Copepoda: Calanoida) in the North Atlantic Ocean. J Exp Mar Biol Ecol 461:479–488. doi:10.1016/j.jembe.2014.10. 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