By increasing local genetic drift and generating inbreeding, population spatial structure may have important effects on the evolutionary benefits of sexual reproduction. In this article, we consider a population structured according to the island model, and use two and three-locus analytical models and multilocus simulations to explore the selective forces acting on a modifier locus affecting the rate of sexual reproduction of facultatively sexual organisms, in the presence of recurrent deleterious mutations. The results show that population structure and selection combine to generate a local excess of heterozygotes at selected loci (negative $F_{\mathrm{IS}}$), for both partially recessive and partially dominant deleterious alleles. The linkage disequilibrium between deleterious alleles may be either negative or positive depending on their dominance coefficient, the degree of population structure and the rate of sex. These genetic associations combine with many other ones to generate indirect selection at the sex modifier locus, generally favoring intermediate rates of sex even when sex entails direct fitness costs. Multilocus simulations show that the equilibrium rate of sex increases moderately as the degree of population structure increases. However, population structure may also prevent the irreversible spread of asexual mutants when the cost of sex is strong. ### Competing Interest Statement The authors have declared no competing interest.

The impact of climate change on populations will be contingent upon their contemporary adaptive evolution. In this study, we investigated the contemporary evolution of 4 populations of the cold-water kelp Laminaria digitata by analyzing their spatial and temporal genomic variations using ddRAD-sequencing. These populations were sampled from the center to the southern margin of its north-eastern Atlantic distribution at 2 time points, spanning at least 2 generations. Through genome scans for local adaptation at a single time point, we identified candidate loci that showed clinal variation correlated with changes in sea surface temperature (SST) along latitudinal gradients. This finding suggests that SST may drive the adaptive response of these kelp populations, although factors such as species' demographic history should also be considered. Additionally, we performed a simulation approach to distinguish the effect of selection from genetic drift in allele frequency changes over time. This enabled the detection of loci in the southernmost population that exhibited temporal differentiation beyond what would be expected from genetic drift alone: these are candidate loci which could have evolved under selection over time. In contrast, we did not detect any outlier locus based on temporal differentiation in the population from the North Sea, which also displayed low and decreasing levels of genetic diversity. The diverse evolutionary scenarios observed among populations can be attributed to variations in the prevalence of selection relative to genetic drift across different environments. Therefore, our study highlights the potential of temporal genomics to offer valuable insights into the contemporary evolution of marine foundation species facing climate change.

Microsatellite data (12 loci) of 14 populations of Laminaria digitata covering the entire species range

Marine ecosystems formed by kelp forests are severely threatened by global change and local coastline disturbances in many regions. In order to take appropriate conservation, mitigation, and restoration actions, it is crucial to identify the most diverse populations which could serve as a “reservoir” of genetic diversity. This requires the development of specific tools, such as microsatellite markers to investigate the level and spatial distribution of genetic diversity. Here, we tested new polymorphic microsatellite loci from the genome of the kelp, Laminaria digitata, and tested them for cross-amplification and polymorphism in four closely related congeneric species (Laminaria hyperborea, Laminaria ochroleuca, Laminaria rodriguezii, and Laminaria pallida). Adding these 20 new microsatellite loci to the ten L. digitata loci previously developed by Billot et al. (Mol Ecol 7:1778-1780, 1998) and Brenan et al. (J R Soc Interface 11:1-12, 2014) and to the ten L. ochroleuca loci previously developed by Coelho et al. (Conserv Genet Resource 6:949-950, 2014), we retained a total of 30 polymorphic loci for L. digitata, 21 for L. hyperborea, 16 for L ochroleuca, 18 for L. rodriguezii, and 12 for L. pallida. These markers have been tested for the first time in the last two species. As predicted, the proportion of markers that cross-amplified between species decreased with increasing genetic distance. In addition, as problems of species identification were reported in this family, mainly between L. digitata and Hedophyllum nigripes, but also between L. digitata, L. hyperborea, and L. ochroleuca in areas where their range distributions overlap, we report a rapid PCR identification method based on species-specific COI mitochondrial primers that allows these four species of kelp to be rapidly distinguished.

Although temporally changing environments generally favor sex and recombination, the effects of spatial environmental heterogeneity have been less explored. In this article, we use a classical model of adaptation along with an environmental gradient to study the selective forces acting on reproductive mode evolution in the central and marginal parts of the distribution range of a species. The model considers a polygenic trait under stabilizing selection (the optimal trait value changing across space) and includes a demographic component imposing range limits. The results show that in the central part of the range (where populations are well adapted), recombination tends to increase the mean fitness of offspring in regimes where drift is sufficiently strong (generating a benefit for sex), while it has the opposite effect when the effect of drift stays negligible. However, these effects remain weak and are easily overwhelmed by slight intrinsic fitness differences between sexuals and asexuals. In agreement with previous results, asexuality may be favored in marginal populations, as it can preserve adaptation to extreme conditions. However, a substantial advantage of asexuality is possible only in conditions maintaining a strong maladaptation of sexuals at range limits (high effective environmental gradient, weak selection at loci coding for the trait).

In the North-east (NE) Atlantic, most intertidal fucoids and warm-temperate kelps show unique low-latitude gene pools matching long-term climatic refugia. For cold-temperate kelps data are scarcer despite their unique cultural, ecological and economic significance. Here we test whether the amphi-Atlantic range ofLaminaria digitatais derived from past glacial survival (and vicariance) in both NE and North-west (NW) Atlantic refugia (as suggested by niche modelling), or post-glacial (re)colonization (as suggested by low mtDNA divergence). We screened 14 populations from across the species range for 12 microsatellite loci to identify and map major gene pools and refugia. We assessed if NW Atlantic survival was supported by unique endemic variation, and if genetic diversity and structure were, as predicted from larger hindcasted glacial ranges, higher in the NE Atlantic. Microsatellite data subdividedL. digitatainto three main genetic groups matching Brittany, northern Europe and the NW Atlantic, with finer-scale sub-structuring within European clusters. The relatively diverse NE Atlantic lineages probably survived the Last Glacial Maximum along unglaciated periglacial shorelines of the Armorican and Celtic Seas (Brittany cluster) and Ireland (northern European cluster), and remain well differentiated despite their relative proximity. The unique Brittany gene pool, at the contemporary European rear edge, is projected to disappear in the near future under high greenhouse gas emission scenarios. Low allelic diversity and low endemism in the NW Atlantic are consistent with recent post-glacial colonization from Europe, challenging the long-standing hypothesis ofin situglacial survival. Confusion withHedophyllum nigripesmay have led to underestimation of regional diversity ofL. digitata, but also to overestimation of its presence along putative trans-Atlantic migration routes. Partial incongruence between modelling and genetic-based biogeographic inferences highlights the benefits of comparing both approaches to understand how shifting climatic conditions affect marine species distributions and explain large-scale patterns of spatial genetic structure.

In recent years, kelp populations worldwide have faced decline and extirpation at their equatorward limits, while models predict a poleward shift of kelp ecosystems during climate change. To gain an understanding of local thermal adaptation and response plasticity in a forest-forming kelp species, we assessed populations of Laminaria digitata along its entire European distribution range for their capacity to withstand high temperature stress, and analysed population structure and diversity with microsatellite markers (n=12). We sampled wild meristematic L. digitata material (n=30) at six locations ranging from Kongsfjorden, Spitsbergen, to the southernmost distribution limit in Quiberon, France. In a heatwave experiment, we subjected samples from all locations to the same, sublethal temperature treatments (15–23°C for eight days including acclimation) and assessed growth, storage compounds, photosynthetic efficiency and pigment contents as response traits. Recovery was assessed following seven days at 15°C. Microsatellite genotyping revealed all sampled populations to be genetically distinct entities, underlying strong regional structuring between southern and northern clades. Genetic diversity was highest at the southern distribution limit in Quiberon and lowest in the geographically isolated population on the island of Helgoland in the North Sea. The physiological response of L. digitata to temperature was similar over the entire distribution range and did not reflect the mean temperature gradient along the latitudinal gradient. However, material from Spitsbergen and Helgoland presented subtle differentiations in their temperature responses, which reflect long-term local temperature histories at these sites. Finally, a heatwave reaching 23°C for five days led to a cessation of growth, from which none of the sampled populations recovered. Our results suggest that the heat stress response of L. digitata is generally stable across its distribution range, despite strong genetic structuring of the populations. Slight local differentiation occurred in populations from the most distinct thermal environments, but 23°C posed a growth limit for all populations. This implies that local adaptation in trailing edge populations of L. digitata might not alleviate detrimental effects of global warming.

Abstract To understand the thermal plasticity of a coastal foundation species across its latitudinal distribution, we assess physiological responses to high temperature stress in the kelp Laminaria digitata in combination with population genetic characteristics and relate heat resilience to genetic features and phylogeography. We hypothesize that populations from Arctic and cold‐temperate locations are less heat resilient than populations from warm distributional edges. Using meristems of natural L. digitata populations from six locations ranging between Kongsfjorden, Spitsbergen (79°N), and Quiberon, France (47°N), we performed a common‐garden heat stress experiment applying 15°C to 23°C over eight days. We assessed growth, photosynthetic quantum yield, carbon and nitrogen storage, and xanthophyll pigment contents as response traits. Population connectivity and genetic diversity were analyzed with microsatellite markers. Results from the heat stress experiment suggest that the upper temperature limit of L. digitata is nearly identical across its distribution range, but subtle differences in growth and stress responses were revealed for three populations from the species’ ecological range margins. Two populations at the species’ warm distribution limit showed higher temperature tolerance compared to other populations in growth at 19°C and recovery from 21°C (Quiberon, France), and photosynthetic quantum yield and xanthophyll pigment responses at 23°C (Helgoland, Germany). In L. digitata from the northernmost population (Spitsbergen, Norway), quantum yield indicated the highest heat sensitivity. Microsatellite genotyping revealed all sampled populations to be genetically distinct, with a strong hierarchical structure between southern and northern clades. Genetic diversity was lowest in the isolated population of the North Sea island of Helgoland and highest in Roscoff in the English Channel. All together, these results support the hypothesis of moderate local differentiation across L. digitata's European distribution, whereas effects are likely too weak to ameliorate the species’ capacity to withstand ocean warming and marine heatwaves at the southern range edge.

Heterosis describes the phenotypic superiority of hybrids over their parents in traits related to agronomic performance and fitness. Understanding and predicting nonadditive inheritance such as heterosis is crucial for evolutionary biology as well as for plant and animal breeding. However, the physiological bases of heterosis remain debated. Moreover, empirical data in various species have shown that diverse genetic and molecular mechanisms are likely to explain heterosis, making it difficult to predict its emergence and amplitude from parental genotypes alone. In this study, we examined a model of physiological dominance initially proposed by Sewall Wright to explain the nonadditive inheritance of traits like metabolic fluxes at the cellular level. We evaluated Wright's model for two fitness-related traits at the whole-plant level, growth rate and fruit number, using 450 hybrids derived from crosses among natural accessions of A. thaliana. We found that allometric relationships between traits constrain phenotypic variation in a nonlinear and similar manner in hybrids and accessions. These allometric relationships behave predictably, explaining up to 75% of heterosis amplitude, while genetic distance among parents at best explains 7%. Thus, our findings are consistent with Wright's model of physiological dominance and suggest that the emergence of heterosis on plant performance is an intrinsic property of nonlinear relationships between traits. Furthermore, our study highlights the potential of a geometric approach of phenotypic relationships for predicting heterosis of major components of crop productivity and yield.