Chaotic Genetic Patchiness in the Highly Valued Atlantic Stalked Barnacle Pollicipes pollicipes From the Iberian Peninsula: Implications for Fisheries Management

Marina Parrondo,Paloma Morán,Lucía García-Flórez,Juliette Chiss,Didier Jollivet,Joana N Fernandes,Nicolas Weidberg,Jose L Acuña,Eva García-Vázquez,Eric Thiébaut,Yaisel J Borrell,Julio Arrontes,Gonzalo Macho,Teresa Cruz,Katja J Geiger,Marion Ballenghien,Alba Aguión

doi:10.3389/fmars.2022.801780

Abstract

The stalked barnacle Pollicipes pollicipes inhabits rocky shores from the Atlantic coasts of Brittany (France) to Senegal. Because of the culinary traditions of southern Europe, stalked barnacles represent an important target species for local fisheries on the Iberian Peninsula. To manage this fishery sustainably, it is therefore important to assess the dynamics of local populations over the Iberian coast, and how they are interconnected at a wider scale using finely tuned genetic markers. In this work, a new enriched library of GT microsatellites for P. pollicipes was prepared and sequenced using Ion Torrent™ Next Gen-Sequencing Technology. 1,423 adults and juveniles were sampled in 15 localities of three geographic regions: southern Portugal, Galicia and Asturias (both in northern Spain). Twenty polymorphic loci arranged in five multiplex PCRs were then tested and validated as new molecular tools to address the spatial and temporal genetic patterns of P. pollicipes. Our results revealed high genetic diversity among adults. However, juveniles were genetically more structured than their adult counterparts, which alternatively displayed much more connectivity among the three studied regions. The lack of spatial genetic heterogeneity in adults may be due to the overlapping of several generations of settlers coming from different geographic origins, which mainly depends on the orientation of residual currents along the coast during reproduction. The genetic differentiation of juveniles may indeed be congruent with Iberian Peninsula hydrodynamics, which can produce chaotic genetic patchiness (CGP) at small temporal scales due to sweepstake reproductive success, collective dispersal and/or self-recruitment. Remarkably, most of the genetic heterogeneity of juveniles found in this work was located in Galicia, which could represent an admixture between distinct metapopulations or an old refuge for the most northern populations. To conclude, high genetic variation in P. pollicipes can lead to the false impression of population panmixia at the Iberian scale by masking more restricted and current-driven larval exchanges between regions. This possibility should be taken into consideration for further specific management and conservation plans for the species over the Iberian Peninsula.

Highlights

The percentage of stocks exploited at biologically unsustainable levels increased from 10% in 1974 to 34.2% in 2017 (FAO, 2020) after decades of management strategies based on catchrate limitations
The typical upwelling circulation during the stalked barnacle larval season in summer/autumn 2017 along the coasts of northern and western Iberia, sea surface temperature (SST) along with modeled sea surface currents datasets revealed that the SST patterns showed strong onshore advection of cold waters (13–15◦C) on the Galician and Portuguese shelves with upwelling filaments extending further offshore especially at the upwelling centers of Fisterra, A Guarda, and Cape da Roca (Figure 1)
P. pollicipes displays high genetic diversity, which is attributable to large effective population sizes representing a well-connected network of local populations

Summary

Introduction

The percentage of stocks exploited at biologically unsustainable levels increased from 10% in 1974 to 34.2% in 2017 (FAO, 2020) after decades of management strategies based on catchrate limitations (i.e., the EU Common Fisheries Policy). As an alternative or complementary approach, management practices are increasingly incorporating the spatial allocation of fishing intensity through marine protected areas, marine zoning, or spatial user rights, for sessile or low-motility species (Lorenzen et al, 2010; Rassweiler et al, 2012). Optimization of these processes depends on the accurate estimation of the connectivity among management units, mediated by the dispersal of the planktonic larval stages (Silva et al, 2019). Advection by ocean currents should lead to long dispersal distances exceeding the scale of management, there is increasing evidence that long-distance dispersal may be rare on ecological time scales (Palumbi, 2003; Selkoe et al, 2010; D’Aloia et al, 2015). An additional line of evidence reveals surprising patterns of spatial and temporal genetic structure observed in some marine species at a scale where genetic variation should be efficiently homogenized by gene flow via larval dispersal, collectively coined chaotic genetic patchiness (CGP) (Johnson and Black, 1982; Hedgecock and Pudovkin, 2011; Eldon et al, 2016)

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