Climatic niche pre-adaptation in mainland Europe facilitated the colonization of Madeira by ivies (Hedera L., Araliaceae)

Abstract

Background and aims: The way plants cope with biotic and abiotic selective pressures determines their success in the colonization of remote oceanic islands, which ultimately depends on the phylogenetic constrains and ecological response of the lineage. In this study we aim to evaluate the relative role of geographical and ecological forces in the origin and evolution of the Madeiran ivy (H. maderensis). Methods: To determine the phylogenetic placement of H. maderensis within the western polyploid clade of Hedera (three species), we analysed 40 populations (92 individuals) using genotyping-by-sequencing and including H. helix as outgroup. Climatic niche differences among the four study species were evaluated using a database with 706 records representing the entire species ranges. To test species responses to climate, a set of 19 vegetative and regenerative functional traits were examined for 70 populations (335 individuals). Key results: Phylogenomic results revealed a nested pattern with H. maderensis embedded within H. iberica. Gradual niche differentiation from the coldest and most continental populations of H. iberica to the warm and stable coastal population sister to H. maderensis parallels the geographical pattern observed in the phylogeny. Similarity in adaptive traits is observed for H. maderensis and H. iberica. The two species show leaves with higher SLA, lower LDMC and thickness and smaller fruits than those of H. hibernica. Conclusions: Acquisition of the Macaronesian climatic niche and the associated functional syndrome in mainland European ivies (small fruits, leaves high SLA, and low LDMD and thickness) was a key step in the colonization of Madeira 1 by the H. iberica/H. maderensis lineage, which points to climatic pre-adaptation as a driver of island colonization (dispersal and establishment). Once in Madeira, speciation was driven by geographical isolation, while ecological processes are regarded as secondary forces with a putative impact in the lack of further in situ diversification.

Repeated asynchronous evolution of single‐species endemics of ivies (Hedera L.) in Macaronesian archipelagos

“…An analysis of the climatic niche of the Madeiran ivy revealed a preference for warm places with high isothermality and humid summers. Interestingly, these climatic preferences largely overlap with those of H. iberica (Alonso et al, 2022).…”

“…A recent phylogenomic study using the next-generation sequencing technique genotyping-by-sequencing (GBS) clarified the phylogenetic placement and colonization history of H. maderensis (Alonso et al, 2022). This study revealed that the Madeiran ivy is phylogenetically nested within the south-western Iberian endemic H. iberica…”

“…This suggested that the climatic niche of H. maderensis was first acquired by its mainland ancestor, thus representing an example of pre-adaptation. The climatic niche similarity between H. maderensis and H. iberica is paralleled by their phenotypic similarity in functional traits (e.g., fruit and seeds dry mass and specific leaf area, Alonso et al, 2022). This pattern of niche conservatism during the evolution of the Madeiran ivy may be related to the lack of island diversification defining single-species endemics.…”

“…Araliaceae, Azores, Canary Islands, climatic niche, genotyping-by-sequencing, Hedera, island colonization, Macaronesia, Madeira, phylogenomics and described a pattern of budding speciation (Alonso et al, 2022), in which a new species is originated without the extinction of the parental species (Mayr & Bock, 2002). An analysis of the climatic niche of the Madeiran ivy revealed a preference for warm places with high isothermality and humid summers.…”

“…A total of 166 samples from 100 locations representing all ivy species were analysed in the phylogenetic study (Figure S1), including 85 new herbarium samples (Data S1) and samples from a previous study (Alonso et al, 2022)…”