The odd one out or a hidden generalist: Hawaiian Melicope (Rutaceae) do not share traits associated with successful island colonization

Abstract

Oceanic islands are unique in their species composition, which is defined by arrival of colonizers via long distance dispersal followed by establishment of species followed in some cases by adaptive radiation. Evolutionary biologists identified traits facilitating successful colonization of islands as including polyploidy, self‐compatibility, herbaceousness and ability for long‐distance dispersal. Successful establishment and evolutionary diversification of lineages on islands often involves shifts to woodiness and shifts in methods of outcrossing as well as changes in dispersal ability. The genus Melicope colonized numerous archipelagos throughout the Pacific including the Hawaiian Islands, where the lineage comprises currently 54 endemic species and represents the largest radiation of woody plants on the islands. The wide distributional range of the genus illustrates its high dispersibility, most likely due to adaption to bird dispersal. Here we investigate ploidy in the genus using flow cytometry and chromosome counting. We find the genus to be paleopolyploid with 2n = 4x = 36, a ploidy level characterizing the entire subfamily Amyridoideae and dating back to at least the Palaeocene. Therefore Hawaiian Melicope have not undergone recent polyploidization prior to colonization of the islands. Thus Melicope retained colonization success while exhibiting a combination of traits that typically characterize well established island specialists while lacking some traits associated to successful colonizers.

Phylogeny of Hawaiian Melicope (Rutaceae): RAD-seq Resolves Species Relationships and Reveals Ancient Introgression

“…M. hivaoaensis represents an adaptive radiation of five species endemic to the Marquesas Islands, whose predecessor colonized from the Hawaiian Islands (Appelhans et al, 2014a; Appelhans et al, 2018a). Successful island colonizations have been associated with recent hybridization or polyploidization events (Paetzold et al, 2018). There was no polyploidization event immediately prior to the colonization of the Hawaiian Islands itself (Paetzold et al, 2018), making a polyploidization event prior to the colonization of the Marquesas Islands unlikely.…”

“…Synthesizing the unique aspects of island evolution and extrapolating results to larger scales may allow us to better uncover general patterns and processes in evolution. Such phenomena include identifying factors affecting successful colonization and adaptive radiation (Carlquist, 1967; Carlquist, 1974; Paetzold et al, 2018), morphological or ecological shifts (e.g., “insular woodiness”; Carlquist, 1974; Lens et al, 2013), the spatiotemporal origins of lineages (Appelhans et al, 2018a), reconstructing colonization events (Harbaugh et al, 2009), and studying co-evolution (Roderick, 1997). These insights may result in further questions regarding taxonomy, species richness, medicinal or technical applications, and conservation (e.g., Francisco-Ortega et al, 2000).…”

“…In contrast, molecular phylogenetic studies have revealed that many enigmatic Hawaiian plant radiations colonized the islands only once followed by adaptive radiation: the Hawaiian lobeliads (Campanulaceae; Givnish et al, 2009), Psychotria (Rubiaceae; Nepokroeff et al, 2003), Silene (Caryophyllaceae; Eggens et al, 2007), Touchardia/Urera (Urticaceae; Wu et al, 2013), and Melicope (Harbaugh et al, 2009; Appelhans et al, 2014a). Polyploidization and hybridization events were also discovered to predate colonization and radiation in several island lineages, including the Hawaiian silverswords (Asteraceae; Baldwin and Sanderson, 1998; Barrier et al, 1999) and mints (Lamiaceae; Roy et al, 2015) along with the Pan- Pacific sandalwoods (Santalaceae; Harbaugh, 2008), suggesting evolutionary success in young hybrid or polyploid colonists (Carr, 1998; Paetzold et al, 2018).…”

“…In contrast to other successful island radiations, the colonization of the Hawaiian Archipelago in Melicope was not preceded by a recent polyploidization event. In general, the genus Melicope shows a uniform chromosome number (Paetzold et al, 2018). To date, phylogenetic relationships in Hawaiian Melicope have been investigated in four molecular studies (Harbaugh et al, 2009; Appelhans et al, 2014a; Appelhans et al, 2014b; Appelhans et al, 2018a), with a combination of up to six nuclear and plastid genomic regions amplified using polymerase chain reaction.…”

Advances in biogeography in the age of a new modern synthesis

“…We hope that this set of papers will stimulate empirical studies as well as the development of methods for integrative biogeographic studies that simultaneously incorporate several lines of evidence, such as phylogenetic/phylogenomic relationships, divergence times, geographic range evolution, functional traits, and ecology, through Bayesian approaches to test biogeographic hypotheses at various scales (Harris et al, ; Hearn et al, ; Paetzold et al, ; Ree & Sanmartín, ; Klaus & Matzke, ).…”