Spatio-temporal patterns of genetic variation of the silverside Odontesthes regia in the highly productive Humboldt Current System

Highlights

• Populations of Odontesthes regia have high genetic diversities and large effective sizes.

• A biogeographic break around 30°S shapes population dynamics of O. regia.

• O. regia presents co-distributed genetic groups along its distribution range.

• Demographic history of O. regia was shaped by changes in the Humboldt Current.

• No interannual influence of El Niño on the genetic variation of O. regia from 2013 to 2018.

Abstract

The Humboldt Current System (HCS) is characterised by latitudinal upwelling differences and interannual El Niño events that bring equatorial warm waters into the system. Within the HCS, the silverside Odontesthes regia is a coastal fish that faces intense harvesting, and physical and oceanographic variability. Here, we evaluated how different processes in the HCS have shaped the spatial and temporal genetic variation of O. regia populations by using 650-bp alignment of the mitochondrial control region and nine microsatellite loci. We found that both DNA markers indicated high genetic diversity, presence of at least two co-distributed genetic groups, and a slight genetic structure shaped by a biogeographic break within the HCS rather than the latitudinal upwelling differences or geographical distances. Demographic history of these groups suggests an allopatric origin and posterior reconnection as the result of historical changes in the HCS. No genetic interannual divergences were found in subsystems with intermittent presence of warm waters, suggesting no significant influence of El Niño on the genetic variation of O. regia from 2013 to 2018. Despite the inherent disturbances of the HCS, past and recent estimates of effective population sizes showed high values in most populations. Our results provide essential information for the management of O. regia in the HCS. Our study also helps to understand how the spatio-temporal dynamics of the HCS influences the genetic variation of coastal marine fishes.

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.