Hierarchical genetic structuring in the cool boreal kelp, Laminaria digitata: implications for conservation and management

Abstract

Kelp are foundation species threatened by ongoing warming trends and increased harvesting pressure. This emphasizes the need to study genetic structure over various spatial scales to resolve demographic and genetic processes underpinning resilience. Here, we investigate the genetic diversity in the kelp, Laminaria digitata, in previously understudied southern (trailing-edge) and northern (range-centre) regions in the Northeastern Atlantic Ocean. There was strong hierarchical spatial structuring with significantly lower genetic variability and gene flow among southern populations. As these span the area of the Hurd’s deep Pleistocene glacial refuge, the current low variation likely reflects a fraction of previous levels that has been eroded at the species southern edge. Northern variability and private alleles also indicate contributions from cryptic northern glacial refugia. Contrary to expectations of a positive relationship between neutral genetic diversity and resilience, a previous study reported individuals from the same genetically impoverished southern populations to be better adapted to cope with thermal stress than northern individuals. This not only demonstrates that neutral genetic diversity may be a poor indicator of resilience to environmental stress but also confirms that extirpation of southern populations will result in the loss of evolved, not just potential, adaptations for resilience.

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

“…Recently, [ 28 ] challenged the existing paradigm that Arctic marine kelp forests are a depauperate extension of temperate populations and instead emphasized the persistence of Arctic refugia through the cycles of glaciation. 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 : [ 29 , 30 , 31 , 32 ]; L. hyperborea : [ 29 , 33 , 34 ]; L. ochroleuca : [ 14 ]; Saccorhiza polyschides : [ 27 ]; Saccharina latissima : [ 34 , 35 , 36 , 37 , 38 ]). All of these studies agreed that the levels of connectivity were generally very low.…”

“…This implied that the negative consequences of the threats brought about by climate change cannot be mitigated by population connectivity, which makes the scenario of extirpation of a large number of populations and hence widespread loss of genetic diversity highly likely. In this context, populations located in the central part of a species’ distribution range (i.e., the more genetically diverse populations) are generally considered to be less vulnerable to the predicted warming trends compared to the marginal populations (that may already be genetically depauperate) ( L. digitata : [ 32 , 39 ]; Sargassum fallax and Scytothalia dorycarpa : [ 40 ]). The extent of local adaptation depends on a complex balance between selection, drift, and gene flow.…”

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

“…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.…”

“…In this context, populations located in the central part of a species distribution range (i.e. the more genetically diverse populations) are generally considered to be less vulnerable to the predicted warming trends compared to the marginal populations (that may already be genetically depauperate) (L. digitata: [28,35]; Sargassum fallax and Scytothalia dorycarpa: [36]. The extent of local adaptation depends on a complex balance between selection, drift and gene flow.…”

“…Selection is more effective in large, well-connected populations because drift is reduced, but on the other hand gene flow, by reintroducing "poorly adapted genes", can restrict local adaptation. However, even in small populations, the effect of genetic drift can be counterbalanced in a highly selective marginal environment, and local adaptation processes might be favoured [28,35].…”