Global biogeography and diversification of a group of brown seaweeds (Phaeophyceae) driven by clade‐specific evolutionary processes

Abstract

Aim Historical processes that shaped current diversity patterns of seaweeds remain poorly understood. Using Dictyotales, a globally distributed order of brown seaweeds as a model, we test if historical biogeographical and diversification patterns are comparable across clades. Dictyotales contain some 22 genera, three of which, Dictyota, Lobophora and Padina, are exceptionally diverse. Specifically, we test whether the evolutionary processes that shaped the latitudinal diversity patterns in these clades are in line with the tropical conservatism, out‐of‐the‐tropics or diversification rate hypotheses. Location Global coastal benthic marine environments. Taxon Dictyotales (Phaeophyceae). Methods Species diversity was inferred using DNA‐based species delineation, addressing cryptic diversity and circumventing taxonomic problems. A six‐gene time‐calibrated phylogeny, distribution data of 3,755 specimens and probabilistic modelling of geographical range evolution were used to infer historical biogeographical patterns. The phylogeny was tested against different trait‐dependent models to compare diversification rates for different geographical units as well as different thermal affinities. Results Our results indicate that Dictyotales originated in the Middle Jurassic and reach a current peak of species diversity in the Central Indo‐Pacific. Ancestral range estimation points to a southern hemisphere origin of Dictyotales corresponding to the tropical southern Tethys Sea. Our results demonstrate that diversification rates were generally higher in tropical regions, but increased diversification rates in different clades are driven by different processes. Our results suggest that three major clades underwent a major diversification burst in the early Cenozoic, with Dictyota and Padina expanding their distribution into temperate regions while Lobophora retained a predominantly tropical niche. Main conclusions Our results are consistent with both the tropical conservatism hypothesis, in which clades originate and remain in the tropics (Lobophora), and the out‐of‐the‐tropics scenario, where taxa originate and expand towards the temperate regions while preserving their presence in the tropics (Dictyota, Padina).

Global biodiversity patterns of marine forests of brown macroalgae

“…Centres of higher species richness were found in the north-east Pacific (≤ 32 species of kelps) and south-east Australia (≤ 53 species of fucoids). These hotspots differ from those identified previously for the predominantly tropical macroalgal orders Bryopsidales (Indo-Australian Archipelago; Kerswell, 2006) and Dictyotales (Central Indo-Pacific; Vieira et al, 2021) and also between intertidal and subtidal species, consistent with the geography of their evolutionary origin. In contrast, poor-spots of species richness coincided between kelps and fucoids (e.g., higher latitudes; Figures 2a and 3a), in line with previous studies (Kerswell, 2006;Vieira et al, 2021).…”

“…These hotspots differ from those identified previously for the predominantly tropical macroalgal orders Bryopsidales (Indo-Australian Archipelago; Kerswell, 2006) and Dictyotales (Central Indo-Pacific; Vieira et al, 2021) and also between intertidal and subtidal species, consistent with the geography of their evolutionary origin. In contrast, poor-spots of species richness coincided between kelps and fucoids (e.g., higher latitudes; Figures 2a and 3a), in line with previous studies (Kerswell, 2006;Vieira et al, 2021). In the same way, regions with high endemicity coincided for kelps and fucoids, mainly identified in climatically stable and isolated regions of the Galapagos Islands, Antarctica, South Africa, Japan and East Russia (Sakhalin and Kuril Islands; Figures 2b and 3b; Harrison & Noss, 2017).…”

“…Species richness and endemicity by latitudinal bins of 0.5° resolution are presented in the side graphs. Estimates of endemicity have been log 10 transformed to enable the visualization of the zero-skewed values of low (L) and high (H) levels of endemicity regimes and extensive ice coverage Kerswell, 2006;Vieira et al, 2021).…”

“…Additional studies have been conducted at the genus level, which is not necessarily representative of the overall biodiversity (Keith et al., 2014; Kerswell, 2006). Besides, distinct lineages of macroalgae are expected to have distinct richness and endemicity patterns, reflecting their evolutionary histories and tendencies to retain or evolve macroecological preferences (Keith et al., 2014; Verbruggen et al., 2009; Viera et al, 2021).…”

Diversity and taxonomic revision of tribes Rhipileae and Rhipiliopsideae (Halimedaceae, Chlorophyta) based on molecular and morphological data

“…Finally, phylogenetic inference has also been used to decipher biogeographical history, using distribution data to estimate the lineages evolution in space and time (e.g., Vieira et al. 2017, 2021, Leliaert et al. 2018).…”