Independent homoploid hybrid speciation events in the Macaronesian endemic genusArgyranthemum

Abstract

Well‐characterized examples of homoploid hybrid speciation (HHS) are rare in nature, yet they offer the potential to study a number of evolutionary processes. In this study, we investigate putative homoploid hybrid species in the genus Argyranthemum (Asteraceae), a group of plants endemic to the Macaronesian archipelagos of the North Atlantic Ocean. We specifically address a number of knowledge gaps surrounding the origin(s) of A. sundingii and A. lemsii, which are thought to be derived from the same parental cross. Comparisons of leaf morphology suggest that A. sundingii and A. lemsii are distinct from their parental progenitors and distinguishable from each other based on leaf area. Ecological niche modelling (ENM) demonstrated that the homoploid hybrid species occupy novel habitats that are intermediate relative to the parental species. Nuclear simple sequence repeat markers (SSRs) and single nucleotide polymorphism (SNP) data indicate that the homoploid hybrid species are distinct from the parental taxa, while population‐level sampling of chloroplast SSRs and approximate Bayesian computation show that A. sundingii and A. lemsii are independently derived from the same parental cross. As such, Argyranthemum represents an example of independent homoploid hybrid speciation events with evidence of divergence in leaf morphology and adaptation to novel intermediate habitats. On oceanic islands, which are often typified by steep ecological gradients and inhabited by recently derived species with weak reproductive barriers, multiple HHS events from the same parental cross are not only possible but also likely to have played a more important role in oceanic island radiations than we currently think.

Geographical isolation, habitat shifts and hybridisation in the diversification of the Macaronesian endemic genus Argyranthemum (Asteraceae)

“…Using partitioned D‐statistics, which are less susceptible to false positives, hybridisation was supported in in 52% (11/21) of tests performed on Tenerife, one of three tests on La Palma, the single test on El Hierro (1/1) and one of three tests in Gran Canaria. Taken together with evidence that hybridisation has generated two species by homoploid hybrid speciation (Brochmann et al ., 2000; Fjellheim et al ., 2009; White et al ., 2018), it is clear that hybridisation has played a significant role in the evolutionary history and diversification of Argyranthemum , a pattern consistent with the findings in Micromeria (Curto et al ., 2017).…”

“…Samples of all Argyranthemum taxa recognised by Humphries (1976) and Francisco‐Ortega et al . (1996b) were included in our study (Table 1) with the exception of A. sundingii and A. lemsii which are of hybrid origin (Brochmann et al ., 2000; Fjellheim et al ., 2009; White et al ., 2018) and likely to confound phylogenetic analyses (Gruenstaeudl et al ., 2017; McVay et al ., 2017). ‘ Argyranthemum vincentii ’ has been identified in previous studies as an endemic to Tenerife and restricted to pine forest habitats (Francisco‐Ortega et al ., 1996c, 2000) and can be distinguished from closely related taxa by filiform leaf lobes and green (not glaucous) leaves (pers.…”

Insights into genomic structure and evolutionary processes of coastal Suaeda species in East Asia using cpDNA, nDNA, and genome-wide SNPs

“…S1). Homoploid hybrid speciation promoted by ecological selection has been described in several studies and reviews [42][43][44] . In a review by Gross and Rieseberg 42 , the authors explained that homoploid hybrid derivatives resulting from hybridization between parental species may have transgressive traits that can facilitate adaptation to extreme habitats where tolerance of the hybrids exceeds that of the parental species.…”

Island floras as model systems for studies of plant speciation: Prospects and challenges

“…Several homoploid hybrid species in oceanic islands are worthy of study. The genus Argyranthemum (Asteraceae) in the Canary Islands has been particularly well studied (Brochmann, ; Francisco‐Ortega et al, ; Brochmann et al, ; Borgen et al, ; Fjellheim et al, ), and it continues to be investigated (e.g., White et al, ). Very briefly, two described homoploid hybrid species, Argyranthemum lemsii and A. sundingii, have the same parental taxa ( A. frutescens and A. broussonetii ).…”

“…The many markers generated with HTS should provide more definitive evidence for the origins of the hybrid populations (White et al, ). It is perhaps of greater interest to examine the genomic composition of plants in each hybrid population, both those recognized as species and the smaller, presumably hybrid swarm populations.…”