Abstract
The genus Porphyra sensu lato (Bangiaceae, Rhodophyta), an important seaweed grown in aquaculture, is the most genetically diverse group of the Class Bangiophyceae, but has poorly understood genetic variability linked to complex evolutionary processes. Genetic studies in the last decades have largely focused on resolving gene phylogenies; however, there is little information on historical population biogeography, structure and gene flow in the Bangiaceae, probably due to their cryptic nature, chimerism and polyploidy, which render analyses challenging. This study aims to understand biogeographic population structure in the two abundant Porphyra species in the Northeast Atlantic: Porphyra dioica (a dioecious annual) and Porphyra linearis (protandrous hermaphroditic winter annual), occupying distinct niches (seasonality and position on the shore). Here, we present a large-scale biogeographic genetic analysis across their distribution in the Northeast Atlantic, using 10 microsatellites and cpDNA as genetic markers and integrating chimerism and polyploidy, including simulations considering alleles derived from different ploidy levels and/or from different genotypes within the chimeric blade. For P. linearis, both markers revealed strong genetic differentiation of north-central eastern Atlantic populations (from Iceland to the Basque region of Northeast Iberia) vs. southern populations (Galicia in Northwest Iberia, and Portugal), with higher genetic diversity in the south vs. a northern homogenous low diversity. For. P. dioica, microsatellite analyses also revealed two genetic regions, but with weaker differentiation, and cpDNA revealed little structure with all the haplotypes mixed across its distribution. The southern cluster in P. linearis also included introgressed individuals with cpDNA from P. dioica and a winter form of P. dioica occurred spatially intermixed with P. linearis. This third entity had a similar morphology and seasonality as P. linearis but genomes (either nuclear or chloroplast) from P. dioica. We hypothesize a northward colonization from southern Europe (where the ancestral populations reside and host most of the gene pool of these species). In P. linearis recently established populations colonized the north resulting in homogeneous low diversity, whereas for P. dioica the signature of this colonization is not as obvious due to hypothetical higher gene flow among populations, possibly linked to its reproductive biology and annual life history.
Highlights
Ancient evolutionary lineages are more likely to retain traits and imprints of complex evolutionary histories that challenge the understanding of present population structures in extant species
Genomic DNA was isolated from 238 P. linearis individuals and 152 P. dioica individuals using the LiCl extraction protocol described by Hong et al (1992) as modified by van Oppen et al (1995)
STRUCTURE analysis of all 442 genotypes showed an optimum at K = 2 according to the K criterion (Figure 3), at which the cluster assignments generally aligned with the a priori species delimitations into P. linearis and P. dioica
Summary
Ancient evolutionary lineages are more likely to retain traits and imprints of complex evolutionary histories that challenge the understanding of present population structures in extant species. An example is the case of the Bangiales, a distinctive order that represents an ancient lineage (e.g., Blouin et al, 2011) of morphologically simple red algae prone to complex genomic variability due to chimerism and mixoploidy (Varela-Álvarez et al, 2021) Fossil evidence supports this group as the oldest multicellular eukaryotes with sexual reproduction (Butterfield, 2000), and molecular dating indicates that they diversified approximately 250 million years ago from an origin along eastern Gondwanaland (current New Zealand and Australia), or from the Northwest Pacific (Yang et al, 2018), from where they spread worldwide (Xu et al, 2017). The gametophytes of some species form the most valuable seaweed aquaculture crop (mostly known as “nori” and with a retail value considered to be in excess of $1.3 billion per year, Blouin et al, 2011), which has been harvested and/or cultivated mostly in Japan, China and Korea for more than 1000 years
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