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Map showing the worldwide distribution of Macrocystis ecomorphs and sites where the individuals were collected (also Table S2, see supplementary material).
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The brown alga Macrocystis C. Agardh is widely distributed throughout the cold temperate waters of the Northern and Southern hemispheres, forming ecologically diverse and productive kelp forests. The taxonomy of this alga has been under constant discussion. Since the first description, species have been mostly described by holdfast and blade morpho...
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Citations
... Nevertheless, extremely low resolution in molecular studies of closely related species using single or multigene approaches is not unusual, and it has been reported previously in other algal genera. A single-gene cox1 phylogeny of the Laminariacean genus Macrocystis showed extremely low diversity that supported the recognition of a single species (Macaya & Zuccarello, 2010); however, the use of whole-genome sequencing techniques has uncovered genetic differences that challenge this view, as there might be at least two distinct species (Gonzalez et al., 2023). Likewise, species delimitation in Fucus has proven difficult, as species that are easily recognizable have almost identical sequences using traditional genetic markers such as the cox1, mt23S and mtsp genes and ITS1 and ITS2 rRNA regions (Coyer et al., 2006;Kucera & Saunders, 2008), as it is also the case in Atlantic Sargassum. ...
Sargassum species play a key role in habitat formation in tropical and subtropical regions; however, species identification has been hampered by the phenological plasticity exhibited in response to environmental conditions and life history. Molecular phylogenetics has challenged taxa circumscriptions and proven critical in delimiting species in this genus. Yet, the Atlantic species of Sargassum remain poorly understood, and recent studies have shown low molecular diversity between the species in the NW Atlantic. Here, we expand the taxon sampling to the NE Atlantic to assess the diversity of Sargassum in the Atlantic basin, based on a comprehensive morphological and multigene approach. We selected genes commonly used in delineating species in this genus (ITS2, rbc LS, cox 3, mtsp ) and explored additional markers ( cox 2, nad 6, psb C, clp C, atp B) to infer the phylogenetic relationships between the morphospecies observed in the NE Atlantic. Phylogenetic analyses using single‐gene and multigene alignments including 185 new sequences confirmed the low molecular diversity and supported the distinction of a single clade in Sargassum section Sargassum of N Atlantic benthic species. In contrast, morphological analysis resulted in the identification of 10 species and three new morphospecies that we described here but opt not to equate to species until further molecular evidence is available. Our results were congruent with previous findings from the NW Atlantic and highlight the morphological and ecological diversity of Sargassum in the Atlantic. These results suggest a recent colonization and incipient speciation of Sargassum in the Atlantic basin and showcase the need of further high‐throughput analyses.
... The hemispheres were highly genetically differentiated (FST = 0.71) and moderately genetically diverged (dXY = 0.0077). Within North America there are two giant kelp ecomorphs (integrifolia and pyrifera) whose geographic distributions partly overlap in California : bioRxiv preprint 4 were moderately genetically distinct from BCWA (all integrifolia 11,19 ) (FST = 0.34; dXY = 0.0040; Figure S2). Due to geographic, genetic and ecomorph differences, the remainder of our analyses will focus on BCWA only. ...
Kelp forests are declining in many parts of the northeast Pacific. In small populations, genetic drift can reduce adaptive variation and increase fixation of recessive deleterious alleles, but natural selection may purge harmful variants. To understand evolutionary dynamics and inform restoration strategies, we investigated genetic structure and the outcomes of genetic drift and purging by sequencing the genomes of 429 bull kelp (Nereocystis luetkeana) and 211 giant kelp (Macrocystis pyrifera sensu lato) from the coastlines of British Columbia and Washington. We identified 6-7 geographically and genetically distinct clusters in each species. Low effective population size was associated with low genetic diversity and high inbreeding coefficients (including increased selfing rates), with extreme variation in these genetic health indices among bull kelp populations but more moderate variation in giant kelp. We found no evidence that natural selection is purging putative recessive deleterious alleles in either species. Instead, genetic drift has fixed many such alleles in small populations of bull kelp, leading us to predict (1) reduced within-population inbreeding depression in small populations, which may be associated with an observed shift toward increased selfing rate, and (2) hybrid vigour in crosses between small populations. Our genomic findings imply several strategies for optimal sourcing and crossing of populations for restoration and aquaculture, but which require experimental validation. Overall, our work reveals strong genetic structure and suggests that conservation strategies should consider the multiple health risks faced by small populations whose evolutionary dynamics are dominated by genetic drift.
... Based on published reports, the geographic distributions of "integrifolia-morph" and "pyrifera-morph" are parallel across the equator rather than mirrored, contrary to expectations based on latitudinal gradients of most physical and oceanographic factors (Graham et al., 2007;Macaya & Zuccarello, 2010b). In the Northern Hemisphere, "integrifolia-morph" ranges from mid-to high-latitudes and "pyrifera-morph" from mid-to low-latitudes, but in the Southern Hemisphere "pyrifera-morph" generally occurs at higher latitudes while "integrifolia-morph" dominates at lower latitudes ( Figure 2; Graham et al., 2007;Macaya & Zuccarello, 2010a;Schiel & Foster, 2015). ...
... Ecomorph characterization of individuals was based on holdfast morphology ( Figure 1). "Pyrifera-morph" have conical holdfasts while "integrifolia-morph" have rhizomatous holdfasts (Macaya & Zuccarello, 2010b). In addition, the haptera of "pyrifera-morph" holdfasts arise from all sides of the cylindrical segments, while haptera of "integrifolia-morph" are produced only from the edges along two sides of the flattened holdfast (Setchell, 1932;Womersley, 1954). ...
The two most common ecomorphs of giant kelp, Macrocystis pyrifera and Macrocystis integrifolia, exhibit almost no geographic overlap across their range in the temperate waters of North and South America, with few exceptions such as Stillwater Cove, CA, USA. However, in laboratory settings they are able to interbreed. The mechanism for the morphological variation is unknown, and whether these features are genetically fixed or malleable under different environmental conditions is unclear. Our study, for the first time, directly compared the growth, development, and morphological transformations of the two Macrocystis ecomorphs in a common garden experiment. We experimentally tested the influence of local environment on giant kelp morphology by rearing lab‐cultured embryonic sporophytes from spores released by M. pyrifera and M. integrifolia sporophylls collected from multiple individuals at Stillwater Cove, CA. The spores were cultured in three treatments: “pyrifera‐morph” only, “integrifolia‐morph” only, and mixed (50:50 “pyrifera‐morph”:“integrifolia‐morph” spores). We outplanted the resultant embryonic sporophytes to concrete blocks installed at 7.5–9 m depth in the ocean and monitored the development of the sporophytes over 5 months. Our findings of distinct differences in morphology between the pyrifera‐treatment and integrifolia‐treatment individuals at multiple stages of development including reproductive adults indicates that the morphological differences between the two ecomorphs are genetically determined rather than environmentally induced. We found that primary stipe length and number of branches can be used as diagnostic traits for distinguishing the ecomorphs prior to the stage when adult sporophyte morphology can be definitively characterized. Additionally, no morphological hybrids were observed in the mixed‐treatment, and ultimately the mixed‐treatment individuals were more often categorized as “integrifolia‐morph”‐like than “pyrifera‐morph”‐like.
... Interestingly, this name has not been applied to South African specimens, which have instead been referred to as M. pyrifera by Papenfuss (1942), and as M. angustifolia by Seagrief (1984) and Stegenga et al. (1997). Nevertheless, all 13 species and the species variety have been reduced into a single species (Demes et al. 2009), which was later supported by DNA (Coyer et al. 2001;Macaya and Zuccarello 2010). ...
Kelp forests dominate the western and southwestern coastlines of southern Africa. This expansive ecosystem spreads over two very different ecoregions that are of particular interest to researchers due to the complexities of their physical environment. The mid-to-late 1900s saw a proliferation in pioneering research on southern African kelp forests. Since this period (1970-1989), researchers have published comparatively few seminal studies concerning kelp forest ecology and biological functioning. In light of this deficit, this review synthesised pre-existing research on southern African kelp forests, and highlighted key gaps in the research landscape to spark interest and facilitate new studies. Among several others, key research gaps uncovered by this review include kelp carbon sequestration potential and possible contributions to the blue bioeconomy; deeper exploration into the biological functioning and ecological roles of Macrocysis pyrifera and Ecklonia radiata populations in southern Africa; and the impacts of a changing physical environment on these kelp forests. In light of our rapidly changing climate, filling these gaps will be essential in informing conversations around coastal and marine management decisions and policy.
... Finally, it is worth questioning the contention that E. radiata is the most extensively distributed kelp in the Southern Hemisphere. This claim is debatable, especially when considering the broad distribution of Macrocystis pyrifera (Macaya and Zuccarello, 2010). Confirmed records indicate that E. radiata occurs in the Indo-Pacific (Coleman et al., 2022), whereas M. pyrifera is present along all major continental coastlines in the Southern Hemisphere, encompassing numerous islands in the region (Macaya and Zuccarello, 2010). ...
... This claim is debatable, especially when considering the broad distribution of Macrocystis pyrifera (Macaya and Zuccarello, 2010). Confirmed records indicate that E. radiata occurs in the Indo-Pacific (Coleman et al., 2022), whereas M. pyrifera is present along all major continental coastlines in the Southern Hemisphere, encompassing numerous islands in the region (Macaya and Zuccarello, 2010). These seemingly semantic discrepancies could have been easily avoided through consultation with active researchers in the field. ...
... Currently, the species shows a fragmented distribution throughout the region, which has been proposed to be a long-lasting effect of the unprecedented 1982-83 El Niño-Southern Oscillation (ENSO) event, which decimated local populations and had similar effects in Southern California (Arntz & Tarazona, 1990;Dayton & Tegner, 1984;Glynn, 1988). Extreme events are of special concern, as they can drive range contractions over short temporal scales; future projections predict an increase in ENSO magnitude under greenhouse warming (Cai et al., 2021 (Buschmann et al., 2004;Macaya & Zuccarello, 2010). The long latitudinal extent of the coast of Chile harbors local adaptations to thermal conditions, with larger tolerance ranges in low-latitude populations when compared to higher latitude ones (Buschmann et al., 2004). ...
Worldwide climate-driven shifts in the distribution of species is of special concern
when it involves habitat-forming species. In the coastal environment, large Laminarian
algae—kelps—form key coastal ecosystems that support complex and diverse food
webs. Among kelps, Macrocystis pyrifera is the most widely distributed habitat-forming
species and provides essential ecosystem services. This study aimed to establish the
main drivers of future distributional changes on a global scale and use them to predict
future habitat suitability. Using species distribution models (SDM), we examined the
changes in global distribution of M. pyrifera under different emission scenarios with a
focus on the Southeast Pacific shores. To constrain the drivers of our simulations to
the most important factors controlling kelp forest distribution across spatial scales,
we explored a suite of environmental variables and validated the predictions derived
from the SDMs. Minimum sea surface temperature was the single most important
variable explaining the global distribution of suitable habitat for M. pyrifera. Under
different climate change scenarios, we always observed a decrease of suitable habi-
tat at low latitudes, while an increase was detected in other regions, mostly at high
latitudes. Along the Southeast Pacific, we observed an upper range contraction of
−17.08° S of latitude for 2090–2100 under the RCP8.5 scenario, implying a loss of
habitat suitability throughout the coast of Peru and poleward to −27.83° S in Chile. Along the area of Northern Chile where a complete habitat loss is predicted by our
model, natural stands are under heavy exploitation. The loss of habitat suitability will
take place worldwide: Significant impacts on marine biodiversity and ecosystem func-
tioning are likely. Furthermore, changes in habitat suitability are a harbinger of mas-
sive impacts in the socio-ecological systems of the Southeast Pacific.
... Genetic connectivity on the east coast could be explained by the migration of floating adult M. pyrifera being transported by currents and by a relatively strong connectivity in the past. The former hypothesis is supported by other work, both at a global scale (Assis et al. 2023;Coyer et al. 2001;Macaya 2010;Macaya and Zuccarello 2010b, a) and regionally (Johansson et al. 2015;Camus et al. 2018). In the wild, it is unlikely that genetic exchange among regions can occur through spore dispersal as spores are short-lived and have estimated dispersal distances of <1 km . ...
The giant kelp Macrocystis pyrifera is in global decline as a result of numerous stressors operating on both local and global scales. It is a species that holds significant value in terms of the ecosystem services that it provides and its application in aquaculture. In order to safeguard, restore and utilize this species, it is essential that a sound understanding of genetic structure and diversity is established at scales relevant to local management. Seven microsatellite markers were used to analyze 389 individuals from sites across eight geographical regions in New Zealand. While samples of M. pyrifera from the west coast of the South Island (Fiordland), were genetically isolated, the biogeographic separation of sites along the east coast of New Zealand, between Wellington and Stewart Island, remained unclear due to low genetic differentiation between regions. The greatest genetic diversity was seen in the southeast sites, whereas the northeast had the lowest diversity. This pattern is likely driven by the effects of stressors such as high sea surface temperature in these areas as well as oceanic circulation patterns. A key finding from this work was the significant genetic isolation, and therefore vulnerability of M. pyrifera in the Fiordland population, an area that is being subjected to more intense and longer lasting heatwave events.
... Maximal growth rates for the latter were observed at low temperatures (8 • C) (Buschmann et al., 2004;Macaya and Zuccarello, 2010). The long latitudinal extent of the coast of Chile also generates local adaptations to thermal conditions, with larger tolerance ranges in low-latitude populations compared to higher-latitude ones (Buschmann et al., 2004). ...
Aim: Worldwide climate-driven shifts in the distribution of species is of special concern when it involves habitat-forming species. In the coastal environment, large Laminarian algae – kelps – form key coastal ecosystems that support complex and diverse food webs. Among kelps, Macrocystis pyrifera is the most widely distributed habitat-forming species and provides essential ecosystem services. This study aimed to establish the main drivers of future distributional changes on a global scale and use them to predict both future habitat suitability. Location: Global Methods: Using species distribution models (SDM), we examined the changes in global distribution of M. pyrifera under different emission scenarios with a focus on the Southeastern Pacific shores. To constrain the drivers of our simulations to the most important factors controlling kelp forest distribution across spatial scales, we explored a suite of environmental variables and validated the predictions derived from the SDMs. Results: Minimum sea surface temperature was the single most important variable explaining the global distribution of suitable habitat for M. pyrifera . Under different climate change scenarios, we always observed a decrease of suitable habitat at low latitudes, while an increase was detected in other regions, mostly at high latitudes. Along the Southeast Pacific, we observed an upper range contraction of -17.08°S of latitude for 2100 under the RCP8.5 scenario, implying a loss of habitat suitability throughout the coast of Peru and poleward to -27.83°S in Chile. Along the area of Northern Chile where a complete habitat loss is predicted by our model, natural stands are under heavy exploitation. Main conclusions: The loss of habitat suitability will take place worldwide: significant impacts on marine biodiversity and ecosystem functioning are likely. Furthermore, changes in habitat suitability are a harbinger of massive impacts in the socio-ecological systems of the Southeastern Pacific.
... Currently, the species shows a fragmented distribution throughout the region, which has been proposed to be a long-lasting effect of the unprecedented 1982-83 El Niño-Southern Oscillation (ENSO) event, which decimated local populations and had similar effects in Southern California (Arntz & Tarazona, 1990;Dayton & Tegner, 1984;Glynn, 1988). Extreme events are of special concern, as they can drive range contractions over short temporal scales; future projections predict an increase in ENSO magnitude under greenhouse warming (Cai et al., 2021 (Buschmann et al., 2004;Macaya & Zuccarello, 2010). The long latitudinal extent of the coast of Chile harbors local adaptations to thermal conditions, with larger tolerance ranges in low-latitude populations when compared to higher latitude ones (Buschmann et al., 2004). ...
Worldwide climate-driven shifts in the distribution of species is of special concern when it involves habitat-forming species. In the coastal environment, large Laminarian algae – kelps – form key coastal ecosystems that support complex and diverse food webs. Among kelps, Macrocystis pyrifera is the most widely distributed habitat-forming species and provides essential ecosystem services. This study aimed to establish the main drivers of future distributional changes on a global scale and use them to predict future habitat suitability with a focus on the southeastern Pacific coast. Using species distribution models (SDM), we examined the changes in global distribution of M. pyrifera under different emission scenarios. To constrain the drivers of our simulations to the most important factors controlling kelp forest distribution across spatial scales, we explored a suite of environmental variables and validated the predictions derived from the SDMs. Minimum sea surface temperature was the most important variable explaining the global distribution of suitable habitat for M. pyrifera . Under different climate change scenarios, we always observed a decrease of suitable habitat at low latitudes, while an increase was detected in other regions, mostly at high latitudes. Along the southeast Pacific, we observed a range contraction of 14.5 of latitude for 2100 under the RCP 8.5 scenario, implying a loss of habitat suitability throughout the coast of Peru and poleward to 27.83S in Chile. On the northern coast of Chile, the area coinciding with the complete habitat loss predicted by our model is under heavy exploitation with over 11,180 tons harvested every year from natural populations of M. pyrifera . The loss of habitat suitability will likely have significant impacts on marine biodiversity and ecosystem functioning and is a harbinger of massive impacts in the socio-ecological systems of the southeastern Pacific.
... However, the morphological variability is probably driven by environmental effects on the early development of the sporophytes, and all species have collapsed into M. pyrifera (Demes, Graham, & Suskiewicz, 2009). Posterior DNA barcoding studies supported the recognition of a single species (Macaya & Zuccarello, 2010a). This taxonomic revision turned M. pyrifera into the only kelp present in both the northern and southern hemispheres. ...
... Although there is a broader distribution of M. pyrifera across the southern hemisphere, there is only information on mitochondrial and chloroplast genomes from individuals from the northern hemisphere. Overall, there have been few genetic studies surveying giant kelp populations from the southern hemisphere, and these were based on a few molecular markers or microsatellites (Astorga, Hernández, Valenzuela, Avaria-Llautureo, & Westermeier, 2012;Camus, Faugeron, & Buschmann, 2018;Coyer, Smith, & Andersen, 2001;Durrant, Barrett, Edgar, Coleman, & Burridge, 2015;Macaya & Zuccarello, 2010a, 2010b. These molecular markers, especially the organellar genes cox1 and rbcL, showed a low divergence between giant kelp populations (Durrant, Barrett, Edgar, Coleman, & Burridge, 2015). ...
... We reconstructed a haplotype network for the cytochrome c oxidase subunit I gene (cox1) to investigate the origin of M. pyrifera in France. We extracted the partial cox1 sequence from the mitochondrial genome of the French specimen and aligned it with cox1 sequences obtained by Macaya and Zuccarello (2010a) and Durrant, Barrett, Edgar, Coleman, and Burridge (2015). The reconstruction was performed with the minimum spanning method using PopART v.17 (Leigh, Bryant, Nakagawa, & Nakagawa, 2015). ...
Macrocystis pyrifera is a foundation species that creates kelp forests and supports essential ecosystem services across coastal environments. Over the past half-century, more than 95% of giant kelp forests have declined around Tasmania and Australia due to climate change, causing a near-complete loss of the ecosystems and services they support. Compared with northern hemisphere giant kelp ecosystems, Australian populations have received little research attention in genomic and other genetic analyses. We present the complete mitochondrial and chloroplast genomes of Macrocystis pyrifera from Tasmania. Both organellar genomes were similar to published Laminariales genomes in length, GC content, gene composition and synteny. A phylogeny constructed by combining protein-coding genes from both genomes showed Tasmanian specimens clustered with M. pyrifera specimens from the northern hemisphere. Genetic differences in protein genes between the Tasmanian M. pyrifera and the northern hemisphere specimens were overall low, but some ribosomal protein genes presented higher values of nonsynonymous mutations. The most divergent gene, the mitochondrial conserved hypothetical protein ORF377, can provide insights into the evolution of the species. This gene has been proposed as a suitable molecular marker for population genetic research in Fucales and may also be helpful for intraspecific studies of M. pyrifera. The complete mitochondrial and chloroplast genomes of Tasmanian M. pyrifera provide important genetic data and critical information for further evolutionary and population studies and for managing these endangered and disappearing populations.
