Pre‐Pleistocene origin of phylogeographical breaks in African rain forest trees: New insights from Greenwayodendron (Annonaceae) phylogenomics

Abstract

Aim Palaeoecological records indicate that Pleistocene glaciations affected the African rain forest, probably causing its fragmentation, which could explain phylogeographical breaks documented in many tree species. This refuge hypothesis was further tested through species distribution models, hindcasting persistence during the Last Glacial Maximum. However, previous studies failed to estimate with sufficient precision the divergence time between phylogeographical entities to confirm their Pleistocene origin. Developing genomic tools on a representative tree of mature rain forests, we test if parapatric genetic clusters documented in widespread tree species can be interpreted as the legacy of past population fragmentation during the last glacial period(s). Location Tropical Africa, Guineo‐Congolian forests. Taxon Greenwayodendron (Annonaceae). Methods To further test the Pleistocene refuge hypothesis by molecular dating, we sequenced the plastome of 145 individuals of the shade‐tolerant rain forest tree Greenwayodendron suaveolens and congeneric species, and genotyped the same samples using nuclear microsatellites to identify genetic clusters. Results Five plastid phylogroups of G. suaveolens occur in parapatry throughout Central Africa, following a spatial pattern generally congruent with genetic clusters. Four of them diverged 3.5–4.5 Ma, whereas the fifth one, located in the Cameroon volcanic line (CVL), diverged 8.3 Ma, in the range of divergence times between Greenwayodendron species, highlighting the key role of the CVL in hosting ancient lineages. Within phylogroups, most nodes were dated from 0.9 to 3.2 Myr and a correlation between haplotype divergence and spatial distance was still perceptible, indicating a slow population dynamic. Main conclusions The phylogeographical structures of Central African trees probably established during the Pliocene or early Pleistocene, and while they might have been reinforced during subsequent glacial–interglacial cycles, interglacial phases did not lead to genetic homogenization. Therefore, interpreting phylogeographical patterns of African trees must account for a much deeper past than previously assumed, and cannot be limited to the last glacial period.

Population genomics of the widespread African savannah treesAfzelia africanaandAfzelia quanzensisreveals no significant past fragmentation of their distribution ranges

“…In general, this genetic structuring cannot be explained by current geographic barriers such as the main mountain chains (Cameroonian Volcanic Line, Cristal Mountains, and Chaillu massif) or major rivers in the region (Sanaga, Dja, and Oougué Rivers). Molecular dating suggests historical isolation of the tree populations, probably led by rainforest fragmentation, during the cold, dry Ice‐Age periods of the Pleistocene (<2.58 million years ago; Piñeiro et al., ; Demenou et al., ), but possibly even earlier (Migliore et al., ). These results contrast with the genetic connectivity found for the Afzelia and other savannah tree species over large Sudanian and Zambezian ranges.…”

“…In the last few years, population genetic data have accumulated for a number of African rainforest trees and revealed well-differentiated parapatric genetic clusters in Central and West African rainforests for most species (e.g., Budde et al, 2013;Hardy et al, 2013;Daïnou et al, 2014Daïnou et al, , 2016Heuertz et al, 2014;Piñeiro et al, 2017;Demenou et al, 2018;Migliore et al, 2018). In general, this genetic structuring cannot be explained by current geographic barriers such as the main mountain chains (Cameroonian Volcanic Line, Cristal Mountains, and Chaillu massif) or major rivers in the region (Sanaga, Dja, and Oougué Rivers).…”

Species delimitation in the genus Greenwayodendron based on morphological and genetic markers reveals new species

“…usambaricum at the rank of species. This is in fact also supported by plastid and nuclear DNA sequences indicating that Usambaricum does not fall within the clade including all Suaveolens (Couvreur & al., ; Migliore & al., ).…”

Reticulate evolution as a management challenge: Patterns of admixture with phylogenetic distance in endemic fishes of western North America

“…The western North American monsoon was severely depressed by glaciation (Bhattacharya, Tierney, Addison, & Murray, 2018), such that summer temperatures in the continental interior averaged 8-14°C below contemporary levels, while plant communities were depressed 600- with an extensive Holocene drought (Sullivan et al, 2016). These climatic effects were global in nature and greatly impacted aquatic and terrestrial fauna beyond Western North America (Brunner, Douglas, & Bernatchez, 1998;Brunner, Douglas, Osinov, Wilson, & Bernatchez, 2001;Bryson, Murphy, Lathrop, & Lazcano-Villareal, 2011;Migliore et al, 2019;Morales-Barbero, Martinez, Ferrer-Castán, & Olalla-Tárraga, 2018).…”