Climatic niche pre-adaptation facilitated island colonization followed by budding speciation in the Madeiran ivy (Hedera maderensis, Araliaceae)

Abstract

The path followed by species in the colonization of remote oceanic islands ultimately depends on their phylogenetic constraints and ecological responses. In this study, we aim to evaluate the relative role of geographical and ecological forces in the origin and evolution of the Madeiran ivy (Hedera maderensis), a single-species endemic belonging to the western polyploid clade of Hedera. To determine the phylogenetic placement of H. maderensis within the western polyploid clade, we analyzed 40 populations (92 individuals) using genotyping-by-sequencing and including Hedera helix as outgroup. Climatic niche differences among the study species were evaluated using a database with 867 records representing the entire species ranges. To test species responses to climate, 13 vegetative and reproductive functional traits were examined for 70 populations (335 individuals). Phylogenomic results revealed a nested pattern with H. maderensis embedded within the south-western Iberian 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 functional traits is observed for H. maderensis and H. iberica. The two species show leaves with higher specific leaf area (SLA), lower leaf dry matter content (LDMC) and thickness and fruits with lower pulp fraction than the other western polyploid species H. hibernica. Acquisition of a Macaronesian climatic niche and the associated functional syndrome in mainland European ivies (leaves with high SLA, and low LDMC and thickness, and fruits with less pulp content) was a key step in the colonization of Madeira by the H. iberica/H. maderensis lineage, which points to climatic pre-adaptation as key in the success of island colonization (dispersal and establishment). Once in Madeira, budding 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

“…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). We included 62 individuals from 33 populations of Macaronesian ivies: 19 individuals of H. azorica (12 populations), 19 individuals of H. canariensis (11 populations) and 24 individuals of H. maderensis (10 populations).…”

“…We used 500 ng of DNA per sample to prepare a GBS library. We replicated five samples and included four replicates of samples included in Alonso et al (2022) to confirm their consistent phylogenetic placement within and between libraries. For library preparation, we followed Fernández‐Mazuecos et al (2018), based on Elshire et al (2011) with modifications (Escudero et al, 2014; Grabowski et al, 2014).…”

“…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). This suggested that the climatic niche of H. maderensis was first acquired by its mainland ancestor, thus representing an example of pre‐adaptation.…”

“…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 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.…”

“…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.…”