Ecology and genetics underlying local adaptation to global change across life stages of dominant kelp species

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Publications

Editorial: Opening the black box of kelps: Response of early life stages to anthropogenic stressors

Publication . Martins, Neusa; Coleman, Melinda A.; Wernberg, Thomas; Roleda, Michael Y.

Kelps form marine forests along world’s coastlines, providing valuable ecosystem goods and services, either directly as a source offood or medicinal products, or indirectly as biogenic habitats or carbon sink agents (Teagle et al., 2017; Wernberg et al., 2019). However, kelp forests are currently under threat due to anthropogenic climate change with latitudinal range shifts and large-scale declines at a global scale (Smale et al., 2019; Wernberg et al., 2019). Most studies on the impact of anthropogenic stressors on kelps have focused on the macroscopic sporophyte stage of the haploid-diploid life cycle (Schiel and Foster, 2006; Veenhof et al., 2022). However, the microscopic stages considered as the “black box” of kelps due to the complexity of studying them in situ, have been suggested to play a crucial role in the persistence of populations that experience sporophyte mortality after large-scale disturbances (McConnico and Foster, 2005; Barradas et al., 2011) as they can persist as “seed bank” analogues under adverse conditions (Hoffmann and Santelices, 1991; Veenhof et al., 2022). This Research Topic is a collection of 8 articles contributing to opening the “black box” of kelps by providing greater insight into how microscopic life stages of kelps are affected by anthropogenic climate change, helping to predict the persistence of these foundation species and therefore the fate of ecosystems and coastal communities. These studies highlight that the response of kelp early life stages to stressors can be strongly dependent on the population and thermal history.

2023-01Journal article

Open Access

Microscopic life stages of Arctic kelp differ in their resilience and reproductive output in response to Arctic seasonality

Publication . Silva, Cláudio Figueira; Pearson, Gareth; Serrao, Ester; Bartsch, Inka; Martins, Neusa

Kelp forests are important habitats in the strongly environmentally and seasonally variable Arctic. There is a critical lack of knowledge about how seasonal conditions and climate change scenarios influence survival and reproduction of kelp early life stages. To better understand the regulation of kelp life cycle processes in this harsh environment we focused on the physiological performance and reproductive success of early life stages in Alaria esculenta and Laminaria digitata from Kongsfjorden, Spitsbergen. Gametophyte growth and survival during Arctic winter and subsequent sporophyte recruitment under spring conditions were investigated. Winter conditions (2 degrees C, complete darkness) halted gametophyte growth and prevented the onset of gametogenesis in both species. The gametophytes of L. digitata but not A. esculenta became fertile after returning to spring conditions, suggesting that sporogenesis, sexual reproduction and recruitment in A. esculenta must occur successively during summer/autumn while in L. digitata a new generation of sporophytes could develop from over-wintering gametophytes. The effects of simulated canopy shading (offering protection against extreme irradiance stress, particularly as sea ice retreats), present-day and projected Arctic summer seawater temperatures, and nutrient levels on gametophyte survival, fertility and sporophyte recruitment success were also investigated in both species. A. esculenta gametophytes had greater survival and reproductive success than L. digitata, except under very low light (simulating dense canopy). In contrast, shading was required for reproductive success in L. digitata gametophytes. Predicted summer temperatures of 9 degrees C reduced sexual reproduction in both species. Interactions observed between these environmental drivers probably reflect species-specific seasonal patterns of survival and reproduction. These differences between kelp species in response to abiotic factors and light levels (simulated canopy shading) suggest that climate change could alter community structure in the Arctic through effects on sexual reproduction and sporophyte recruitment success. HIGHLIGHTS center dot Gametophytes were able to endure long periods of darkness.center dot Parental kelp canopy is key for gametophyte survival and recruitment.center dot Climate change may alter kelp recruitment patterns.

2022Journal article

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A novel sexual system in male gametophytes of Laminaria pallida (Phaeophyceae)

Publication . Liboureau, Pierre; Pearson, Gareth; Serrao, Ester; Kreiner, Anja; Martins, Neusa

Brown algae (Phaeophyceae) exhibit a wide diversity of sexual systems, reproductive modes and life histories. The evolution of this diversity has often involved transitions between sexual systems, which may influence genetic diversity and diversification, and phenotypic evolution. This study reports a novel sexual system in kelp. We identified male gametophyte strains of Laminaria pallida that, despite presenting morphological features typical of a male, developed both antheridia and egg-like structures, which suggest an incomplete suppression of femaleness during sexual determination of gametophytes. The sperm released by these variant male gametophytes successfully fertilize eggs produced by female gametophytes, developing into sporophytes with normal morphologies. However, morphologically abnormal sporophytic offspring were formed in isolated variant male gametophytes, indicating that the egg-like structures were not successfully self-fertilized by sperm. The causes of the unsuccessful intragametophytic selfing are unknown, but absence of pheromone production by the egg-like structures is a hypothesis suggested by available evidence. Partial co-sexuality is clearly inherited, as all male gametophyte strains descended from the same sporophyte developed egg-like structures. Further investigation into the genetics and maturation of male partheno-sporophytes will help to estimate the potential effects of this mechanism on natural populations.

2024Journal article

Open Access

A low‐latitude species pump: Peripheral isolation, parapatric speciation and mating‐system evolution converge in a marine radiation

Publication . Almeida, Susana C.; Neiva, João; Sousa, Filipe; Martins, Neusa; Cox, Cymon; Melo‐Ferreira, José; Guiry, Michael D.; Serrao, Ester; Pearson, Gareth

Geologically recent radiations can shed light on speciation processes, but incomplete lineage sorting and introgressive gene flow render accurate evolutionary reconstruction and interpretation challenging. Independently evolving metapopulations of low dispersal taxa may provide an additional level of phylogeographic information, given sufficiently broad sampling and genome-wide sequencing. Evolution in the marine brown algal genus Fucus in the south-eastern North Atlantic was shaped by Quaternary climate-driven range shifts. Over this timescale, divergence and speciation occurred against a background of expansion-contraction cycles from multiple refugia, together with mating-system shifts from outcrossing (dioecy) to selfing hermaphroditism. We tested the hypothesis that peripheral isolation of range edge (dioecious) F. vesiculosus led to parapatric speciation and radiation of hermaphrodite lineages. Species tree methods using 876 single-copy nuclear genes and extensive geographic coverage produced conflicting topologies with respect to geographic clades of F. vesiculosus. All methods, however, revealed a new and early diverging hermaphrodite species, Fucus macroguiryi sp. nov. Both the multispecies coalescent and polymorphism-aware models (in contrast to concatenation) support sequential paraphyly in F. vesiculosus resulting from distinct evolutionary processes. Our results support (1) peripheral isolation of the southern F. vesiculosus clade prior to parapatric speciation and radiation of hermaphrodite lineages-a "low-latitude species pump". (2) Directional introgressive gene flow into F. vesiculosus around the present-day secondary contact zone (sympatric-allopatric boundary) between dioecious/hermaphrodite lineages as hermaphrodites expanded northwards, supported by concordance analysis and statistical tests of introgression. (3) Species boundaries in the extensive sympatric range are probably maintained by reproductive system (selfing in hermaphrodites) and reinforcement.

2022Journal article

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