Spatio-temporal patterns of genetic variation of the silverside Odontesthes regia in the highly productive Humboldt Current System
Graphical Abstract
Introduction
Oceans are known to present physical barriers such as intrinsic oceanographic features (Von der Heyden et al., 2011), upwelling cells (Henriques et al., 2014), and biogeographic barriers (Briggs and Bowen, 2012, Teske et al., 2011), which are capable of disrupting gene flow while genetically structuring marine populations. Consequently, genetic structure in marine realms can be found in spatially separated populations (McKeown et al., 2019), slightly connected populations forming metapopulations (Steneck and Wilson, 2010), or even mixed populations (i.e., sympatric, Sanchez et al., 2020). These genetically mixed populations represent a challenge for researchers and stakeholders because the conditions that promoted their genetic divergence cannot be easily identified or are currently absent.
The Humboldt Current System (HCS) is one of the most productive eastern boundary upwelling systems in the world (Montecino and Lange, 2009). It spans from northern Peru (~4°S) where cold upwelled waters encounter warm tropical waters, to the south of Chile (~45°S) where interacts with an estuarine basin, the Inner Sea of Chiloe (Fig. 1). A division of three subsystems has been suggested in the HCS due to the dissimilar upwelling intensity levels: a permanently productive northern subsystem (NS) (4–13°S), a large central upwelling subsystem (CS) (15–26°S), and a seasonally productive southern subsystem (SS) (south of the 34°S) (Montecino and Lange, 2009). The spatial upwelling variation of the HCS is greatly influenced by El Niño-Southern Oscillation (ENSO), whose warm phase (El Niño) interannually brings low-oxygen equatorial warm waters to the upwelling areas off Peru (Arntz et al., 2006), producing changes in biomass and distribution of several marine species (Estrella and Swartzman, 2010). Under this scenario, populations would find their genetic make-up variable. Hence, both spatial and temporal genetic studies in species along the HCS are imperative.
At the HCS, historical and contemporary factors such as upwelling cells (Tarazona and Arntz, 2001, Thiel et al., 2007), nearshore thermal discontinuities (30–31°S) (Tapia et al., 2014), biogeographic breaks (~30°S and 42°S) (Camus, 2001), and the scarce to narrow continental shelf at north of 32°S (Thiel et al., 2007), favoured the retention and dispersal of several species, shaping their population abundances and genetic structure (Haye et al., 2014, McKeown et al., 2019). Among all these factors, the biogeographic break (~30°S) between the CS and SS have left a strong genetic signature in many invertebrate and seaweed species (Macaya and Zuccarello, 2010, Martin and Zuccarello, 2012, Haye et al., 2014, McKeown et al., 2019), which found their dispersal potential reduced by oceanographic and physical conditions associated to this break. In addition, studies of historical demography in the HCS have suggested demographic expansion in different species (Barahona et al., 2017, Pardo-Gandarillas et al., 2018, McKeown et al., 2019) that are concordant with changes in sea surface temperature (SST), primary production, fluctuations in the intensity of El Niño events, and sea-level changes during the glaciation and deglaciation events of the Late Pleistocene and Holocene (Hulton et al., 2002, Rein et al., 2005). Also, studies that assessed the genetic variation of fishes in the HCS are limited to few harvested pelagic fishes (e.g., Cárdenas et al., 2009; Barahona et al., 2017). However, how the historical events, interannual oscillations, and inherent HCS’s oceanography variability influence the genetic variation of coastal marine fishes remains unknown.
The silverside, Odontesthes regia, is a coastal fish distributed along the HCS, from northern Peru to southern Chile (Dyer, 2006). All Pacific Ocean members of the genus Odontesthes have originated in southern Chile (Hughes et al., 2020) but O. regia is the only species with a wide northward geographic distribution (Dyer, 2006). This species is an asynchronous multiple-spawner with large spawning seasons (Plaza et al., 2011) and a maximum lifespan of four years. Fishery landings of O. regia are negatively affected by interannual El Niño events (Estrella and Swartzman, 2010), probably related to warm conditions (Santoso et al., 2017, Echevin et al., 2018), which occurs in some congeners (Strüssmann et al., 2010). The spatial differences of upwelling intensity along the HCS influence this species. In fact, there is evidence that this variability could have promoted morphometric and meristic differences in O. regia (Deville et al., 2020). These characteristics and the distribution of O. regia along the HCS make it a suitable model to understand the influence of the spatial and temporal changes of the HCS on the patterns of genetic variation of coastal fishes.
Here, we use the hypervariable mitochondrial control region and nuclear microsatellite loci to investigate the genetic structure and diversity of O. regia along most of the distribution range, and the interannual genetic variation in the northern and central subsystems, which are highly influenced by El Niño events. We also estimated migration rates, time of historical demographic fluctuations, contemporary patterns of genetic variation, and effective population sizes. Our findings are useful to understand the influence of past and current spatio-temporal processes of the HCS on the population dynamics and dispersion of coastal fishes. Furthermore, the information generated here can be used to improve management policies in O. regia.
Section snippets
Sampling
We collected 462 individuals from the northernmost to southernmost extension of the HCS, off Peru and Chile. This sampling covered a largely described biogeographic break at 30°S and the three upwelling subsystems of the HCS: the northern subsystem (NS), the central subsystem (CS), and the southern subsystem (SS) (Fig. 1). Our sampling included the following locations: Puerto Rico (PRI), Chimbote (CHI) and Lagunilla (LAG) in the NS; Chala (CHA), Ilo (ILO) and Iquique (IQQ) in the CS; and Lo
Results
We detected a total of 186 haplotypes in 413 sequences (GenBank accession numbers: MT899507–MT899919). All locations showed values of haplotype and nucleotide diversity higher than 0.94 and 0.08, respectively (Table 1). A total of 357 individuals were genotyped with SSRs. These loci showed values of allele richness and heterozygosity higher than 15 and 0.8, respectively (Table 1). Genetic indexes from SSRs in each location are shown in detail in Table A2.
Discussion
We evaluated the influence of both the spatial and interannual dynamics of the Humboldt Current System on the genetic variation of the silverside Odontesthes regia. In general, populations of O. regia had high genetic diversity, which agrees with values found in congeners inhabiting other oceanic systems (Beheregaray and Sunnucks, 2001, Cocito et al., 2019); and coastal pelagic species distributed in the HCS (Cárdenas et al., 2009, Barahona et al., 2017, McKeown et al., 2019). These high values
Conclusion
We used mitochondrial and microsatellites DNA markers to describe how O. regia responded to the historical processes and contemporary spatio-temporal variation of the HCS. Patterns from both DNA markers showed slight significant divergences between populations at north and south of a biogeographic break present around the 30°S, and at least two co-distributed genetic groups along the HCS. Demographic history suggests the allopatric formation of these groups after the formation of the break and
CRediT authorship contribution statement
D. Deville, G. Sanchez, S. Barahona, and D. Oré-Chávez conceived of the initial idea. D. Deville, G. Sanchez, S. Barahona, D. Oré-Chávez, and T. Umino designed the methodology. D. Deville collected samples, carried out experiments and performed statistical analyses. D. Deville, G. Sanchez, S. Barahona, R. Quiroz Bazán, D. Oré-Chávez and T. Umino verified the statistical analyses and supervised the experiments. C. Yamashiro, R. Quiroz Bazán, and D. Oré-Chávez encouraged D. Deville to investigate
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This study was financed by the Japanese Government through the Ministry of Education, Culture, Sport, Science, and Technology (MEXT) and the Research Vice-rectorate of the Universidad Nacional Mayor de San Marcos (Grant ID: 151001077) in Lima, Peru. We would like to thank to Kevin Ttito and all the IMARPE personnel who kindly helped with the sampling of individuals from Peru.
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