Strong population structure but no equilibrium yet: Genetic connectivity and phylogeography in the kelp Saccharina latissima (Laminariales, Phaeophyta)

Abstract

Kelp aquaculture is globally developing steadily as human food source, along with other applications. One of the newer crop species is Saccharina latissima, a northern hemisphere kelp inhabiting temperate to arctic rocky shores. To protect and document its natural genetic variation at the onset of this novel aquaculture, as well as increase knowledge on its taxonomy and phylogeography, we collected new genetic data, both nuclear and mitochondrial, and combined it with previous knowledge to estimate genetic connectivity and infer colonization history. Isolation‐with‐migration coalescent analyses demonstrate that gene flow among the sampled locations is virtually nonexistent. An updated scenario for the origin and colonization history of S. latissima is developed as follows: We propose that the species (or species complex) originated in the northwest Pacific, crossed to the northeast Pacific in the Miocene, and then crossed the Bering Strait after its opening ~5.5 Ma into the Arctic and northeast Atlantic. It subsequently crossed the Atlantic from east to west. During the Pleistocene, it was compressed in the south with evidence for northern refugia in Europe. Postglacial recolonization led to secondary contact in the Canadian Arctic. Saccharina cichorioides is shown to probably belong to the S. latissima species complex and to derive from ancestral populations in the Asian North Pacific. Our novel approach of comparing inferred gene flow based on coalescent analysis versus Wright's island model suggests that equilibrium levels of differentiation have not yet been reached in Europe and, hence, that genetic differentiation is expected to increase further if populations are left undisturbed.

Seascape Genomics of the Sugar Kelp Saccharina latissima Along the North Eastern Atlantic Latitudinal Gradient

“…The location of the ice-free refugia a species was occupying during the LGM is likely to have had a major influence on the genetic diversity patterns observed across that species' present-day range [3,23]. As the global scale phylogeography of S. latissima has not as of yet been completely resolved [34,40], the precise location of the LGM refugia of this species is open to speculation. Our results suggest support for the existence of the Iberian Peninsula S. latissima LGM refugia due to the observed pattern of strong genetic differentiation among the southernmost populations (see below).…”

“…latissima is a cold-tolerant species, the potential localization of its ice age refugia even further north [34,76] should also be taken into account. Indeed, a recent meta-analysis of multiple cold-tolerant seaweed species (including S. latissima) found elevated levels of genetic diversity within the Arctic populations of many of these species, suggesting that in some cases it may have even been possible for the species to persist at high latitudes throughout the LGM [76].…”

“…The general trend revealed a reduction in genetic diversity with increasing latitude that was linked with episodes of contraction/expansion of the species' ranges during the Last Glacial Maximum (LGM) [6,23,24]. In addition, levels of connectivity between marine forests of a number of European kelp species have been investigated at different spatial scales ranging from less than 1 km to in excess of hundreds of kilometers (Laminaria digitata: [25][26][27][28]; L. hyperborea: [25,29,30]; L. ochroleuca: [11]; Saccorhiza polyschides: [24]; Saccharina latissima: [29,[31][32][33][34]. All of these studies agreed that the levels of connectivity were generally very low.…”

Marine stepping‐stones: Connectivity of Mytilus edulis populations between offshore energy installations

“…Convergence of estimated parameter distributions was ensured by: checking effective sample size (ESS) values, autocorrelation values and chain swapping, exam-ining trend line plots for absence of trends, and comparing parameter estimates generated from the genealogies produced during the first and second half of runs. A mutation rate for the seven microsatellite loci of 0.001564 per generation was assumed, following the methodology ofLuttikhuizen et al (2018). Migration rates among sampled locations were visualized by chord diagrams using the r package circlize version 0.4.3(Gu, Gu, Eils, Schlesner, & Brors, 2014).The fit of the pairwise isolation-with-migration models to the data and the underlying processes was assessed by comparing the distribution of estimated migration rates with that of the pairwise F ST values directly estimated from the microsatellite data.…”

Cultivar Development of Kelps for Commercial Cultivation—Past Lessons and Future Prospects

“…Recently, a number of population genetic analyses using molecular marker data have been conducted in order to describe the geographical pattern of genetic variation in kelp species. For example, based on microsatellite data, it has been shown that there is statistically significant genetic differentiation among both European and North-American populations of S. latissima, at least at distances above around 100 km (Guzinski et al, 2016;Nielsen et al, 2016;Paulino et al, 2016;Breton et al, 2018;Evankow et al, 2018;Luttikhuizen et al, 2018;Mooney et al, 2018). In spite of the genetic differentiation between populations, analysis of molecular variance indicated that most of the genetic variation (>90%) was found within populations rather than between populations (Breton et al, 2018;Mooney et al, 2018).…”