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.
Highlights
Understanding the processes driving speciation in marine ecosystems remained a challenge until recently, due to the unclear nature of dispersal boundaries
Much marine diversity stems from climate-driven vicariant and colonization events [2,3], the accumulation of phylogenetic information is revealing that a considerable amount of diversity arises during adaptive radiations [4,5], these periods of rapid
Mating system and reproductive ecology can play an important role in marine speciation (e.g., [14]), they remain under-studied in this environment
Summary
Understanding the processes driving speciation in marine ecosystems remained a challenge until recently, due to the unclear nature of dispersal boundaries. Recent evidence for marine adaptive radiations and ecological speciation, as well as previously undetected patterns of cryptic speciation is overturning this view. Most of the world’s biodiversity occurs in the oceans, but understanding the processes that drive speciation in marine ecosystems remains a challenge due to the perceived scarcity of geographical barriers to gene flow [1]. Mating system and reproductive ecology can play an important role in marine speciation (e.g., [14]), they remain under-studied in this environment. The evolutionary shift toward selfing increases colonization potential and reproductive assurance, while serving to maintain local adaptations in stressful environments at the cost of genetic diversity and evolvability [16]
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