Pleistocene population expansions of shade-tolerant trees indicate fragmentation of the African rainforest during the Ice Ages

Abstract

The fossil record in tropical Africa suggests that dry conditions during the Ice Ages caused expansion of savannahs and contraction of the rainforest. Forest refugia have been proposed to be located in areas of Central Africa that currently harbour high rates of endemic species. However, to what extent the forest was fragmented remains unknown. Nuclear microsatellites and plastid sequences of 732 trees of two species occurring in the same habitat-mature lowland evergreen rainforests-but with remarkably different dispersal capacities-animal versus gravity-were analysed. Geographical information system tools revealed intraspecific lineages partially congruent across the two species, suggesting common past barriers to gene flow in Central Africa. According to approximate Bayesian computation, the intraspecific genetic clusters diverged during the Pleistocene (less than 2 Ma), so that intraspecific differentiation is the appropriate scale to test the aridification effect of the Ice Ages on tree populations. Demographic tests revealed clear genetic signals of population expansion in both taxa, possibly following bottleneck events after forest fragmentation, with stronger evidence of expansion after the Penultimate rather than after the Last Glacial Maximum. The differential dispersal capacity may have modulated the particular response of each species to climate change, as revealed by the stronger evidence of expansion found in the animal-dispersed species than in the gravity-dispersed one.

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

“…The two early‐diverging clades of the tree separated allopatric species that diverged during the mid and late Miocene (Figure a,b), in agreement with current taxonomic status: the West‐African G. oliveri lineage (node A, 11.46 Myr) and the East‐African G. usambaricum (node B, 10.03 Myr). The remaining samples (clade C, 9.03 Myr) included our focal species, G. suaveolens s.s., but also two other sympatric species: (a) G. gabonicum , monophyletic and endemic to Gabon (Piñeiro et al., ), which diverged 8.25 Ma (node E) from a G. suaveolens lineage mainly occurring along the CVL (clade “ G. suav . CP W‐CVL”), and (b) G. glabrum (indicated by * at the tips of Figure a) which is not monophyletic but embedded within G. suaveolens .…”

“…Eight polymorphic nuclear microsatellite (nSSR) loci were amplified in two multiplex reactions as described in Piñeiro, Micheneau, Dauby, and Hardy (), targeting the same samples used for plastomes sequencing from the datasets of Piñeiro et al. () and B.‐J. Lissambou (unpublished data).…”

“…Signatures of fragmentation in Pleistocene forest refugia were then investigated at the intraspecific genetic scale (Hardy et al., ). Using microsatellite and plastid markers, recurrent spatial genetic discontinuities were detected in several tree species, especially among Upper Guinea in West Africa, Lower Guinea in western Central Africa and Congolia in Eastern Central Africa (White, ), but also within these domains (North‐South and/or East‐West subdivisions in Lower Guinea) (Blatrix et al., ; Dauby et al., ; Demenou, Doucet, & Hardy, ; Demenou, Piñeiro, & Hardy, ; Hardy et al., ; Heuertz, Duminil, Dauby, Savolainen, & Hardy, ; Piñeiro, Dauby, Kaymak, & Hardy, ). These patterns provided support for the role of refugia during Pleistocene climate oscillations, as suggested for the Cameroon volcanic line (CVL, Figure b) hosting endemic species and genetic lineages (Dauby et al., ; Maley, ).…”

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

“…For K = 5, under the default setting but with the independent allele frequency model, the a priori group Suaveolens became subdivided into two clusters with many intermediates, corresponding to parapatric clusters described in Piñeiro & al. () for the taxon G. suaveolens subsp. suaveolens var.…”

“…Within each genetic group, the mean observed heterozygosity ( H O ) is lower than the mean expected heterozygosity ( H E ) under Hardy‐Weinberg conditions, leading to positive inbreeding coefficients ( F I ), which probably results from genetic substructure, as observed by Piñeiro & al. () in Suaveolens, but also potentially from the impact of null alleles.…”