TY - JOUR
T1 - Trans-Arctic asymmetries, melting pots and weak species cohesion in the low-dispersal amphiboreal seaweed Fucus distichus
AU - Neiva, João
AU - Assis, Jorge
AU - Fragkopoulou, Eliza
AU - Pearson, Gareth A.
AU - Raimondi, Peter T.
AU - Anderson, Laura
AU - Krause-Jensen, Dorte
AU - Marbà, Núria
AU - Want, Andrew
AU - Selivanova, Olga
AU - Nakaoka, Masahiro
AU - Grant, W. Stewart
AU - Konar, Brenda
AU - Roleda, Michael Y.
AU - Sejr, Mikael K.
AU - Paulino, Cristina
AU - Serrão, Ester A.
N1 - Publisher Copyright:
Copyright © 2024 Neiva, Assis, Fragkopoulou, Pearson, Raimondi, Anderson, Krause-Jensen, Marbà, Want, Selivanova, Nakaoka, Grant, Konar, Roleda, Sejr, Paulino and Serrão.
PY - 2024/4/18
Y1 - 2024/4/18
N2 - Amphiboreal taxa are often composed of vicariant phylogroups and species complexes whose divergence and phylogeographic affinities reflect a shared history of chronic isolation and episodic trans-Arctic dispersal. Ecological filters and shifting selective pressures may also promote selective sweeps, niche shifts and ecological speciation during colonization, but these are seldom considered at biogeographical scales. Here we integrate genetic data and Ecologic Niche Models (ENMs) to investigate the historical biogeography and cohesion of the polymorphic rockweed Fucus distichus throughout its immense amphiboreal range, focusing on trans-Arctic asymmetries, glacial/interglacial dynamics, and integrity of sympatric eco-morphotypes. Populations were sampled throughout the Pacific and the Atlantic, from southern rear-edges to the high-Arctic. They were genotyped for seven microsatellites and an mtDNA spacer, and genetic diversity and structure were assessed from global to local scales. ENMs were used to compare niche divergence and magnitude of post-glacial range shifts in Pacific versus Atlantic sub-ranges. Haplotypic and genotypic data revealed distinct and seemingly isolated Pacific vs Arctic/Atlantic gene-pools, with finer-scale regional sub-structuring pervasive in the Pacific. MtDNA diversity was highly structured and overwhelmingly concentrated in the Pacific. Regionally, Alaska showed the highest intra-population diversity but the lowest levels of endemism. Some sympatric/parapatric ecotypes exhibited distinct genotypic/haplotypic compositions. Strikingly, niche models revealed higher Pacific tolerance to maximum temperatures and predicted a much more consolidated presence in the NE Atlantic. Glacial and modern ranges overlapped extensively in the Pacific, whereas the modern Atlantic range was largely glaciated or emerged during the Last Glacial Maximum. Higher genetic and ecogeographic diversity supports a primary Pacific diversification and secondary Atlantic colonization, also likely reflecting the much larger and more stable climatic refugia in the Pacific. The relic distribution and reduced ecological/morphological plasticity in the NE Atlantic are hypothesized to reflect functional trans-Arctic bottlenecks, recent colonization or competition with congeners. Within the Pacific, Alaska showed signatures of a post-glacial melting pot of eastern and southern populations. Genetic/ecotypic variation was generally not sufficiently discontinuous or consistent to justify recognizing multiple taxonomic entities, but support a separate species in the eastern Pacific, at the southern rear-edge. We predict that layered patterns of phylogeographic structure, incipient speciation and niche differences might be common among widespread low-dispersal amphiboreal taxa.
AB - Amphiboreal taxa are often composed of vicariant phylogroups and species complexes whose divergence and phylogeographic affinities reflect a shared history of chronic isolation and episodic trans-Arctic dispersal. Ecological filters and shifting selective pressures may also promote selective sweeps, niche shifts and ecological speciation during colonization, but these are seldom considered at biogeographical scales. Here we integrate genetic data and Ecologic Niche Models (ENMs) to investigate the historical biogeography and cohesion of the polymorphic rockweed Fucus distichus throughout its immense amphiboreal range, focusing on trans-Arctic asymmetries, glacial/interglacial dynamics, and integrity of sympatric eco-morphotypes. Populations were sampled throughout the Pacific and the Atlantic, from southern rear-edges to the high-Arctic. They were genotyped for seven microsatellites and an mtDNA spacer, and genetic diversity and structure were assessed from global to local scales. ENMs were used to compare niche divergence and magnitude of post-glacial range shifts in Pacific versus Atlantic sub-ranges. Haplotypic and genotypic data revealed distinct and seemingly isolated Pacific vs Arctic/Atlantic gene-pools, with finer-scale regional sub-structuring pervasive in the Pacific. MtDNA diversity was highly structured and overwhelmingly concentrated in the Pacific. Regionally, Alaska showed the highest intra-population diversity but the lowest levels of endemism. Some sympatric/parapatric ecotypes exhibited distinct genotypic/haplotypic compositions. Strikingly, niche models revealed higher Pacific tolerance to maximum temperatures and predicted a much more consolidated presence in the NE Atlantic. Glacial and modern ranges overlapped extensively in the Pacific, whereas the modern Atlantic range was largely glaciated or emerged during the Last Glacial Maximum. Higher genetic and ecogeographic diversity supports a primary Pacific diversification and secondary Atlantic colonization, also likely reflecting the much larger and more stable climatic refugia in the Pacific. The relic distribution and reduced ecological/morphological plasticity in the NE Atlantic are hypothesized to reflect functional trans-Arctic bottlenecks, recent colonization or competition with congeners. Within the Pacific, Alaska showed signatures of a post-glacial melting pot of eastern and southern populations. Genetic/ecotypic variation was generally not sufficiently discontinuous or consistent to justify recognizing multiple taxonomic entities, but support a separate species in the eastern Pacific, at the southern rear-edge. We predict that layered patterns of phylogeographic structure, incipient speciation and niche differences might be common among widespread low-dispersal amphiboreal taxa.
KW - climate-driven range shifts
KW - cryptic species
KW - functional bottleneck
KW - genetic hotspots and melting pots
KW - intertidal
KW - niche unfilling
KW - trans-Arctic phylogeography
UR - http://www.scopus.com/inward/record.url?scp=85192005330&partnerID=8YFLogxK
U2 - 10.3389/fevo.2024.1356987
DO - 10.3389/fevo.2024.1356987
M3 - Article
AN - SCOPUS:85192005330
SN - 2296-701X
VL - 12
JO - Frontiers in Ecology and Evolution
JF - Frontiers in Ecology and Evolution
M1 - 1356987
ER -