Driving south: a multi-gene phylogeny of the brown algal family Fucaceae reveals relationships and recent drivers of a marine radiation

Abstract

BackgroundUnderstanding the processes driving speciation in marine ecosystems remained a challenge until recently, due to the unclear nature of dispersal boundaries. However, recent evidence for marine adaptive radiations and ecological speciation, as well as previously undetected patterns of cryptic speciation is overturning this view. Here, we use multi-gene phylogenetics to infer the family-level evolutionary history of Fucaceae (intertidal brown algae of the northern Pacific and Atlantic) in order to investigate recent and unique patterns of radiative speciation in the genus Fucus in the Atlantic, in contrast with the mainly monospecific extant genera.ResultsWe developed a set of markers from 13 protein coding genes based on polymorphic cDNA from EST libraries, which provided novel resolution allowing estimation of ancestral character states and a detailed reconstruction of the recent radiative history. Phylogenetic reconstructions yielded similar topologies and revealed four independent trans-Arctic colonization events by Fucaceae lineages, two of which also involved transitions from hermaphroditism to dioecy associated with Atlantic invasions. More recently, reversion of dioecious ancestral lineages towards hermaphroditism has occurred in the genus Fucus, particularly coinciding with colonization of more extreme habitats. Novel lineages in the genus Fucus were also revealed in association with southern habitats. These most recent speciation events occurred during the Pleistocene glaciations and coincided with a shift towards selfing mating systems, generally southward shifts in distribution, and invasion of novel habitats.ConclusionsDiversification of the family occurred in the Late-Mid Miocene, with at least four independent trans-Artic lineage crossings coincident with two reproductive mode transitions. The genus Fucus arose in the Pliocene but radiated within a relatively short time frame about 2.5 million years ago. Current species distributions of Fucus suggest that climatic factors promoted differentiation between the two major clades, while the recent and rapid species radiation in the temperate clade during Pleistocene glacial cycles coincided with several potential speciation drivers.

Fucus cottonii(Fucales, Phaeophyceae) is not a single genetic entity but a convergent salt-marsh morphotype with multiple independent origins

“…This genus is an important component of intertidal seaweed assemblages throughout North Atlantic and northeast Pacific shores, colonizing a range of marine and estuarine habitats. It comprises several accepted species divided into two separate lineages: lineage 1 comprises F. serratus and the F. distichus species complex (including F. gardneri from the Pacific); and lineage 2 contains F. ceranoides, F. vesiculosus and F. spiralis, among other species (Serra˜o et al, 1999;Coyer et al, 2006a;Ca´novas et al, 2011). Fucus species typically grow attached to hard substrata by means of an anchoring holdfast, and can generally be differentiated by a variety of ecological, morphological and sexual characters.…”

“…Mitochondrial markers, although often unreliable for determining species relationships in the genus Fucus (Coyer et al, 2006a;Neiva et al, 2010;Ca´novas et al, 2011), indicated that F. cottoniilike forms from the NE Pacific were derived from F. gardneri (Kucera & Saunders, 2008).…”

Unravelling the complexity of salt marsh ‘Fucus cottonii’ forms (Phaeophyceae, Fucales)

“…Two main lineages are apparent within the genus, one consisting of F. distichus L. and F. serratus L. and the other one comprising several species, including F. spiralis L. and F. vesiculosus L., all of which are widespread on shores of the North Atlantic. (Cánovas et al, 2011). Fucus vesiculosus and F. spiralis are closely related and frequently hybridize (Engel et al, 2005), and two new European species within the F. vesiculosus -F. spiralis lineage have been recognized: F. radicans L.Bergstrøm & L.Kautsky from the Baltic Sea (Bergström et al, 2005) and F. guiryi G.I.Zardi, K.R.Nicastro, E.S.Serrão & G.A.Pearson, distributed from Ireland and Britain to the Canary Islands (Zardi et al, 2011).…”

“…Fucus vesiculosus and F. spiralis are closely related and frequently hybridize (Engel et al, 2005), and two new European species within the F. vesiculosus -F. spiralis lineage have been recognized: F. radicans L.Bergstrøm & L.Kautsky from the Baltic Sea (Bergström et al, 2005) and F. guiryi G.I.Zardi, K.R.Nicastro, E.S.Serrão & G.A.Pearson, distributed from Ireland and Britain to the Canary Islands (Zardi et al, 2011). Fucus radicans has evolved in sympatry with F. vesiculosus after the Last Glacial Maximum in Europe (Pereyra et al, 2009), whereas F. guiryi (F. spiralis-south in Coyer et al, 2011) is a sister species of F. spiralis (Cánovas et al, 2011).…”

“…The brown macroalgal genus Fucus is remarkably adaptive and consequently, has evolved into several species in the North Atlantic since the migration of ancestral forms from the North Pacific across the Bering Strait (Cánovas et al, 2011). Two main lineages are apparent within the genus, one consisting of F. distichus L. and F. serratus L. and the other one comprising several species, including F. spiralis L. and F. vesiculosus L., all of which are widespread on shores of the North Atlantic.…”