Recent population expansion in the evolutionary history of the Californian anchovy Engraulis mordax

Expansión poblacional reciente en la historia evolutiva de la anchoveta de California Engraulis mordax

Noé Díaz-Viloria,¹ Laura Sánchez-Velasco¹ and Ricardo Pérez-Enríquez²

¹ Departamento de Plancton y Ecología Pesquera, Centro Interdisciplinario de Ciencias Marinas-Instituto Politécnico Nacional (CICIMAR), Av. Instituto Politécnico Nacional s/n, Col. Playa Palo de Santa Rita, La Paz, B.C.S. 23096, México

Recibido: 31 de octubre de 2011.
Aceptado: 24 de Julio de 2012.

ABSTRACT

The Californian anchovy Engraulis mordax, a temperate species, may have undergone a process of population disjunction from experiencing post-glacial water heating processes around the tip of the Baja California Peninsula, Mexico about 10,000 b.p. A genetic analysis was performed to test the null hypothesis of genetic homogeneity between the Gulf of California and Southern California, U. S. A., and if this is the case, to estimate the time of haplotype emergence in terms of coalescence. A total of 80 sequences of the mtDNA hypervariable control region of E. mordax captured in the central Gulf of California (n = 40) and Southern California (n = 40) were analyzed. In spite of the large number of private haplotypes, no significant genetic differentiation among sites (F_ST = –0.0025, p = 0.686) was observed. An unimodal distribution of mismatch frequency between haplotypes indicated a model of rapid expansion in population size that, based on a mutation rate of 3.6% per million years in the control region, indicates a relatively recent nucleotide differentiation time of approximately 61,000 years. This time period corresponds to the late Pleistocene, suggesting population expansions at each locality, followed by the last episode of glaciation, which may have contributed to migration of this temperate-affinity species between two locations and the genetic homogenization. However this unique recent event of gene flow in the evolutionary history of species does not explain by itself the mismatch distribution patterns found.

Key words: Control region, gene flow, mitochondrial DNA, molecular clock, recent population expansion.

RESUMEN

Palabras clave: ADN mitocondrial, expansión poblacional reciente, flujo genético, región control, reloj molecular.

INTRODUCTION

The Gulf of California is a suggestive model system for studying mechanisms of speciation of marine species by the combination of a relatively large number of endemic species and its geological history (Huang & Bernardi, 2001). The uppermost region of the Gulf of California, Mexico was formed as early as the Miocene, ~25 million years ago. The Baja California Peninsula was then restricted to a small area in the north, and the southern region of the peninsula was composed of several small and large islands, between which several natural seaways connected the Pacific Ocean to the Gulf of California. This situation lasted until ~1 million years ago when the northern peninsula and the southern islands were joined and uplifted to create the present-day Baja California Peninsula (Terry et al., 2000; Huang & Bernardi, 2001; Stepien et al., 2001). Populations of temperate fish species are thought to have been established either by migration, via extinct waterways connecting the Gulf of California to the Pacific Ocean or by migration around the southern tip of Baja California during periods of oceanic cooling associated with glaciating events (Brusca, 1973; Huang & Bernardi, 2001; Bernardi et al., 2003). Presently, gene flow between Pacific and Gulf populations may be limited by physical and physiological barriers (Huang & Bernardi, 2001). If this is the case, then isolation between marine populations in the Gulf of California and the Pacific, based on previous studies, should have occurred between 120,000 and 2.3 million years ago, as suggested for Girella nigricans Ayres 1860 (Terry et al., 2000), Gillichthys mirabilis Cooper 1864 (Huang & Bernardi, 2001), and Paralabrax maculatofasciatus Steindachner 1862 (Stepien et al., 2001).

Among the marine species that may have undergone a population vicariance or disjunction in this region is the Californian anchovy Engraulis mordax Girard, 1854 that is a species of temperate affinity which can be found from Vancouver Island, Canada to the southern part of the Baja California Peninsula (Whitehead et al., 1988), including the Gulf of California (Hammann & CisnerosMata, 1989; Holmgren-Urba & Baumgartner, 1993; Green-Ruiz & Hinojosa-Corona, 1997; Green-Ruiz & Cotero-Altamirano, 2009).

According to genetic variation analysis of cytochrome b of mitochondrial DNA (mtDNA), E. mordax began population expansion 290,000 years ago, and, even though a large percentage of exclusive haplotypes were found at several locations, no significant evidence of disjunction between the subpopulations inside and outside the Gulf of California were reported (Lecomte et al., 2004). Considering that the mtDNA control region shows larger variation than cytochrome b (Rocha-Olivares et al., 1999), it might be a suitable marker not only for genetic differentiation, but to provide an additional estimate on the time of population expansion.

The purpose of this study was to test the null hypothesis of genetic homogeneity between the Gulf of California and Southern California and to reconstruct the evolutionary history of the Californian anchovy E. mordax using the mtDNA hypervariable control region.

MATERIALS AND METHODS

DNA was extracted (Taggart et al., 1992). Concentrations were standardized to 0.05 µg/µL before performing PCR. A fragment of 551 base pairs (bp) of the control region of mtDNA was amplified with primers: FCR2 (5'-ATTTCTGGCCTCTGGTTCCT-3') and RCR2 (5'-CATCTTCAGTGCTATGCTTTG-3') designed for the species (Díaz-Viloria et al., 2005). DNA amplifications were performed in a volume of 25 µL containing 1 µL diluted DNA (0.05 µg/ µL), 0.48 µM of each primer, 80 µM of each dNTP, 0.025 units Taq polymerase (Invitrogen) for Taq buffer 1× (Invitrogen) and 3.5 mM MgCl2. PCR thermal conditions (Progene Thermal Cycler, Techne) were: 2 min at 94 °C, 30 cycles of 1 min at 94 °C, 1 min at 56 °C, 2 min at 72 °C, and a final extension of 4 min at 72 °C.

The PCR products were separated by size on agarose gels (1%) and visualized with SybrGold™. Products with good quality and quantity were cut from the gel, purified (QIAGEN Gel Extraction Kit™) and sequenced in both directions in an automatic sequencer ABI Prism 3730XL (Macrogen, Korea), obtaining two sequences for each individual and a total of 160 sequences for the two locations.

The individual sequences were aligned and checked carefully with CHROMASPRO, vers. 1.34 (McCarty, 1998). The consensus sequences were obtained by reconciling the sequences of the two DNA strands of PCR products that were independently sequenced. The consensus sequences were aligned using Clustal W, vers. 1.83 (Thompson et al., 1994). The sequences of 454 bp of the resulting haplotypes were deposited in GenBank (GU136650GU136673).

Haplotype frequencies were obtained for each location. Genetic diversity was assessed by haplotype diversity (h), nucleotide diversity (π) and nucleotide polymorphism (θ).Tajima's test was performed using DnaSP, vers. 5.10. (Rozas et al., 2003) to determine if mutations are selectively neutral (Tajima, 1989). Population differentiation was assessed between two locations by F_ST (Weir & Cockerham, 1984), based on haplotype frequencies. Significance of population differentiation was assessed by exact test (100,000 steps in Markov chain, 10,000 dememorization steps), and a global AMOVA considering one group of two populations and 50,175 permutations with ARLEQUIN, vers. 3.5 (Excoffier et al., 2005). The gene flow estimate or number of migrant females (Nmf) from DNA sequences was obtained with Equations 3 and 4 from Hudson et al. (1992) with DnaSP, vers. 5.10. A parsimony haplotype network using NETWORK, vers. 4.6.0.0 (Bandelt et al., 1999) was obtained with the control region sequence of Engraulis japonicus Temminck & Schlegel, 1846 (GenBank AB040676) as outgroup. We estimated the time of differentiation between haplotypes (by nucleotide substitution) on a molecular clock of 3.6% per million years (Donaldson & Wilson, 1999). Demographic parameters (τ, θ0, and θ1) from mismatch distributions and fit to a model of rapid population expansion (Rogers & Harpending, 1992) were also obtained with ARLEQUIN, vers. 3.5 (Excoffier et al., 2005). Values of τ from each site were used to estimate the expansion time (T) in the Gulf and Southern California, with the equation T = τ / 2u generations (Rogers & Harpending, 1992), where u was estimated with the equation u = 2µk (Nei & Tajima, 1981), where µ is the mutation rate per nucleotide and k is the number of nucleotides that were covered in the data (454 bp). The divergence rate per nucleotide of 7.2 ×10^–8 per generation (2µ) was obtained considering 3.6% per million years (3.6 × 10^–8) multiplied by two, the generation's time during which every E. mordax individual is sexually mature (Kucas, 1986). Finally, the population size of females before and after population expansion were obtained with the equation N_t = θ_i/2u (Rogers & Harpending, 1992).

RESULTS

The fragment of the mtDNA control region of 80 individuals resulted in 21 variable sites that defined 24 haplotypes, of which 20 (83%) were unique haplotypes for one or another location. The three most frequent haplotypes were shared with similar frequencies between the two locations (Table 1). Tajima's test showed that all mutations were selectively neutral (p > 0.05).

Taking into account a mutational rate of the control region of 3.6% per million years, it is probable that the appearance of haplotypes from HAP6, estimated at 0.22% (one variable site within the 454 bp fragment of the control region) took place ~61,111 (95% CI between 30,254 and 91,968) years ago.

The mismatch distribution was unimodal for the total sample and at both locations, and the observed values fitted simulated values (p > 0.7), indicating rapid expansion in population size, however, slight differences were observed in the modes of mismatch distributions between locations; two pairwise differences were the most frequent in the Gulf of California and one in Southern California (Fig. 3). The estimate of the time of expansion from historical demographic parameters (τ, θ₀, and θ₁) showed consistency with the mutation rate estimate, with values of 43,441 years in Southern California and of 73,911 years in the Gulf of California. The estimate of time of expansion under assumption of two samples as a total population showed a value of 43,074 years. The estimate of female population size before rapid population growth was 9,621, and after rapid population growth, was 107,042. Calculated values are shown in Table 2.

DISCUSSION

Population Genetics. While the lack of significant genetic differentiation between the central Gulf of California and Southern California contrasted with results based on genetic markers of low variability, such as allozymes and proteins (Vrooman et al., 1981; Hedgecock et al., 1989; Hedgecock et al., 1994; Díaz-Jaimes et al., 1999), we confirm the results obtained by Lecomte et al. (2004) who used the mtDNA cytochrome b fraction.

Phylogeography and Historical Gene Flow. The high haplotype diversity (h) and low nucleotide diversity (π) in E. mordax correspond to hypothesis IV (phylogenetic continuity, lack of spatial separation) proposed by Avise et al. (1987), which proposes that species exhibiting this category of intraspecific phylogeography have had relatively extensive and recent historical interconnections through gene flow. This would require the historical absence of firm and longstanding zoogeographic barriers to movement, as well as life histories conducive to dispersal either as pelagic larvae, juveniles, and/or adults.

Low levels of nucleotide diversity (π), mismatch distribution, and star-shaped phylogeny of parsimony network indicate a rapid expansion from a small number of ancestors (Rogers & Harpending, 1992; Grant & Bowen, 1998), which is supported by the negative Tajima's D values, indicating that the population probably experienced a recent bottleneck (Tajima, 1989). According to the estimate of the molecular clock, population expansion may have occurred 61,111 years ago during the late Pleistocene, previous to the last episode of glaciation (Clayton et al., 2006), with a maximum extension (Clark et al., 2009). In this scenario, the rapid population growth would favor retention of new mutations and would be reflected in populations containing one or two predominant haplotypes within a cluster of haplotypes that are one or a few mutations from the central haplotype (Grant & Bowen, 1998). In E. mordax, haplotypes HAP6, HAP2, and HAP18 were the most successful after the bottleneck, and these haplotypes are surrounded by a large number of unique haplotypes. The HAP22 and the group associated with it (H18–H24), despite being the oldest lineages, were less successful than HAP6.

Also, the estimates of expansion time would permit hypothesizing that previous of the last glaciations, E. mordax showed rapid population growth in the Gulf of California 73,911 years ago and in the Southern California 43,441 years ago. During the last glaciations (25,000 years b.p.; Clayton et al., 2006), environmental conditions probably contributed to the dispersal of E. mordax between two regions, improving the levels of gene flow and genetic homogeneity of frequent haplotypes.

The time of coalescence calculated here contrast with the ∼290,000 years (95% CI between 144,000 and 447,000) obtained by Lecomte et al. (2004) for the same species, one half of an order of magnitude greater. Thus, the estimates of control region sequence data suggest a more recent event of rapid population growth ∼61,000 years (95% CI between 30,254 and 91,968) before the present.

About recent historical gene flow, phylogenetic reconstruction (data not shown) and mismatch distribution pattern suggested that last glaciations hypothesis might not be the only event that explains gene flow in E. mordax between Gulf and Southern California. In previous studies where gene flow has been reestablished after divergence of populations into distinct clades, a bimodal pattern of mismatch distribution has been reported (Viñas et al., 2004; Magoulas et al., 2006). In E. mordax such bimodal mismatch distribution was not evident when both samples were analyzed as a total sample. However, differences in the mode of the number of pairwise differences of mismatch distributions between sites probably suggests a first indication of independent demographic histories, in addition to the large number of private haplotypes. But such complete divergence in populations of E. mordax into distinct clades was not demonstrated, probably by insufficient sample size or because the post-glacial water heating process around the tip of the Baja California Peninsula is a very recent event of population disjunction with insufficient time for lineage sorting (Avise, 2000; Freeland, 2007).

In species with high migratory potential, the genetic signal revealing population differentiation is often obscured by population admixture (Alvarado-Bremer et al., 2005). Thus, alternate hypotheses to explain genetic homogeneity in E. mordax between the Gulf and Southern California are sporadic or ongoing gene flow.

Sporadic gene flow. The presence of E. mordax in the Gulf of California, after 1985, probably occurred when a southern subpopulation migrated into the Gulf during anti-El Niño 1986 (Hammann & Cisneros, 1989). This suggestion implies that the Gulf of California stock is an extension of the southern subpopulation. In contrast to this idea, fish scales in anaerobic sediments of the central Gulf of California demonstrated that the anchovy was present in the gulf for at least 250 years and was abundant during the early 18th through early 19th centuries (Holmgren-Urba & Baumgartner, 1993). Those studies and the present suggest the existence of a subpopulation in the Gulf of California which could be connected with a southern subpopulation during periods of cool waters. During anti-El Niño years the southward California current turns westward off-shore typically at Magdalena Bay. At times, however its cool water extend farther south thus permitting southern movement of temperate species that are normally limited to San Lucas Cape; under extreme conditions, California current waters may even enter the Gulf of California (Robles & Marinone, 1987). Although the surface temperatures observed by Hammann & Cisneros (1989), were relatively warm (22-28 °C) for E. mordax, the temperature below the seasonal thermocline might have been cooler. Thus E. mordax appear to enter the Gulf of California during La Niña events. Since 1949 to date, there have been reported six previous intense La Niña events (http://www.esrl.noaa.gov/psd/enso/mei/#data).

Ongoing Gene Flow. Ongoing gene flow between the two regions, as described in other fish species, could be explained by two mechanisms acting together or independently. The first, eggs and larvae could be entrained around San Lucas Cape from or into the Gulf of California, and the second is by migration of adult fish via deeper water (Bernardi et al., 2003).

About the first mechanism, recent zooplankton studies have shown that E. mordax larvae were abundant in Bahía de La Paz during February 2002 (Sánchez-Velasco et al., 2006), at the central region and north of the Gulf of California, during November 1997, December 2002, and February 2006 (Avalos-García et al., 2003; Peguero-Icaza et al., 2008), but were absent at the mouth of Gulf of California, during November 2005 and March 2007 (LeónChávez et al., 2010). In the other hand the hydrography has shown that the Gulf of California is constantly shaken by a wide spectrum of signals coming from the Pacific Ocean. Descriptions of the surface circulations in the Gulf of California suggested inflow in summer and outflow in winter. In the inner mouth there is a clear seasonal cycle, especially in temperature and in mixed layer depth, which varies from 10 m in summer to around 40 m in winter (Lavin & Marinone, 2003). All those studies point to that E. mordax larvae are widely distributed and abundant in the Gulf of California, from Bahía de La Paz, B.C.S. to north of Gulf of California, but it is absent in the mouth of Gulf of California, despite the existence of possible dispersal mechanism during winter. Then it might suggest no larval dispersal around San Lucas Cape, because the presence of fronts, mesoscale structures or thermal barriers (Sánchez-Velasco, pers. comm.), but this hypothesis is recently boarded.

Despite the genetic homogeneity observed in E. mordax between the Gulf of California and the Pacific, it was not possible to distinguish between historical, sporadic or ongoing gene flow events. To test the ongoing gene flow hypothesis (ecological time scale), another sampling design and more rapidly-evolving molecular markers, such as microsatellites, would be required.

Conclusions. Subpopulations of E. mordax in the central Gulf of California and off Southern California probably represent two subunits that are part of a larger population, with sufficient gene flow between them. Mismatch distribution patterns suggest that recent dispersal in the evolutionary history of E. mordax during the last glaciation could contribute to gene flow, but is not the only hypothesis which could explain genetic homogenization, sporadic or ongoing gene flow hypotheses could contribute to a better understanding of genetic similarities of E. mordax at both regions and these must be evaluated.

ACKNOWLEDGMENTS

We thank M. Nevárez-Martínez (CRIP-Guaymas) and J. López-Martínez (CIBNOR-Guaymas) for providing specimens from the central Gulf of California and K. Hill (NOAA) for muscle samples from the San Diego area. Editorial services were provided by I. Fogel of CIBNOR. Thanks to two anonymous referees whose suggestions improved the manuscript. L. Sánchez-Velasco received financial support from the SIP-IPN (2009-2011) and SEP-CONACYT (2008-105922) projects. This article was partly funded by CIBNOR grant EP5.2/2003 to R. Pérez-Enríquez. N. Díaz-Viloria received a fellowship from CONACYT (No. 162710).

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