Alteration of Sexual Reproduction and Genetic Diversity in the Kelp Species Laminaria digitata at the Southern Limit of Its Range

Abstract

Adaptation to marginal habitats at species range-limits has often been associated with parthenogenetic reproduction in terrestrial animals and plants. Laboratory observations have shown that brown algae exhibit a high propensity for parthenogenesis by various mechanisms. The kelp Laminaria digitata is an important component of the ecosystem in Northern European rocky intertidal habitats. We studied four L. digitata populations for the effects of marginality on genetic diversity and sexual reproduction. Two populations were marginal: One (Locquirec, in Northern Brittany) was well within the geographic range, but was genetically isolated from other populations by large stretches of sandy beaches. Another population was at the range limits of the species (Quiberon, in Southern Brittany) and was exposed to much higher seasonal temperature changes. Microsatellite analyses confirmed that these populations showed decreased genetic and allelic diversity, consistent with marginality and genetic isolation. Sporophytes from both marginal populations showed greatly diminished spore-production compared to central populations, but only the southern-limit population (Quiberon) showed a high propensity for producing unreduced (2N) spores. Unreduced 2N spores formed phenotypically normal gametophytes with nuclear area consistent with ≥2N DNA contents, and microsatellite studies suggested these were produced at least in part by automixis. However, despite this being the dominant path of spore production in Quiberon sporophyte individuals, the genetic evidence indicated the population was maintained mostly by sexual reproduction. Thus, although spore production and development showed the expected tendency of geographical parthenogenesis in marginal populations, this appeared to be a consequence of maladaptation, rather than an adaptation to, life in a marginal habitat.

Status, trends and drivers of kelp forests in Europe: an expert assessment

“…The highest abundance of L. digitata and L. hyperborea is found in these two colder regions and correlates with higher genetic diversity, although a trend of decrease in these specieś abundance is revealed for some parts of the central European coasts for small isolated marginal populations (Billot et al 2003;Valero et al 2011;Couceiro et al 2013;Robuchon et al 2014). Signs of maladaptive response (alteration of meiosis) of L. digitata at its southern edge of its distribution (Southern Brittany) became apparent where genetic diversity has declined (Oppliger et al 2014). Such a response means that this European kelp species is at risk of local extinction as predicted by Ecological Niche Models under global change scenarios (Raybaud et al 2013;Assis et al 2016).…”

“…2c). In France, the status of L. digitata remains uncertain but in Brittany some local surveys clearly showed population regressions for small, isolated populations (Couceiro et al 2013) or at their southern range limit (Oppliger et al 2014), with no evident link to harvesting (Valero et al 2011, Derrien-Courtel pers. comm.).…”

Past climate changes and strong oceanographic barriers structured low‐latitude genetic relics for the golden kelp Laminaria ochroleuca

“…This refugium was the northern range margin during colder periods (like the LGM, Figure b) and is presently the southern range margin of the continuous continental distribution. Thus, it might have experienced genetic drift and bottlenecks owing to reduced population sizes while occurring near niche thresholds (Eckert, Samis, & Lougheed, ; Oppliger et al., ). Even when climate conditions in this region approximated niche optimum, priority colonization effects (Neiva et al., ; Tellier, Tapia, Faugeron, Destombe, & Valero, ) and/or strong oceanographic barriers (see discussion below) could have limited gene flow from richer populations.…”

Parthenogenesis is rare in the reproduction of a sexual field population of the isogamous brown alga Scytosiphon (Scytosiphonaceae, Ectocarpales)

“…A dominance of zygotic sporophytes (i.e., rare parthenosporophytes) has also been reported in the sexual populations of Laminaria digitata , Lessonia nigrescens , Dictyosiphon foeniculaceus and Ectocarpus (Peters and Müller , Oppliger et al. , , Couceiro et al. ).…”