Marc S. Appelhans

Collections-based systematics: Opportunities and outlook for 2050

Systematic biology is a discipline rooted in collections. These collections play important roles in research and conservation and are integral to our efforts to educate society about biodiversity and conservation. Collections provide an invaluable record of the distribution of organisms throughout the world and through recent and geological time, and they are the only direct documentation of the biological, physical, and cultural diversity of the planet: past, present, and future. Recent developments in bioinformatics and cyberinfrastructure are transforming systematics by opening up new opportunities and as a result major digitization efforts have increasingly made available large amounts of biodiversity data. The collections‐based systematics community needs to train the next‐generation of systematists with integrative skills, address grand questions about biodiversity at different scales, develop a community‐wide cyberinfrastructure, effectively disseminate systematic data to biologists and the public, and proactively educate the public and policy makers on the importance of systematics and collections in the biodiversity crisis of the Anthropocene. Specifically, we call for a new global Biodiversity CyberBank, comparable to GenBank for genetic data, to be the repository of all biodiversity data, as well as a World Organization of Systematic Biology to lead major initiatives of the field. We also outline a new workflow for taxonomic monographs, which utilizes both the traditional strengths of synthesizing diverse collections‐based taxonomic data and the capacity of online resources and bioinformatics tools.

A molecular phylogeny of Acronychia, Euodia, Melicope and relatives (Rutaceae) reveals polyphyletic genera and key innovations for species richness

We present the first detailed phylogenetic study of the genus Melicope, the largest genus of the Citrus family (Rutaceae). The phylogenetic analysis sampled about 50% of the 235 accepted species of Melicope as well as representatives of 26 related genera, most notably Acronychia and Euodia. The results based on five plastid and nuclear markers have revealed that Acronychia, Euodia and Melicope are each not monophyletic in their current circumscriptions and that several small genera mainly from Australia and New Caledonia need to be merged with one of the three genera to ensure monophyly at the generic level. The phylogenetic position of the drupaceous Acronychia in relation to Melicope, which has capsular or follicular fruits, remains unclear and Acronychia might be a separate genus or a part of Melicope. The seed coats of Melicope, Acronychia and related genera show adaptations to bird-dispersal, which might be regarded as key innovations for species radiations. Euodia and its relatives, which lack these adaptations, include only about 20 species while the Melicope-Acronychia group consists of about 340 species. The drupaceous genera Comptonella, Dutaillyea, Picrella and Sarcomelicope are nested within Melicope and need to be merged with Melicope. The expanded genus is a prime example of the artificial classification system of Engler, who defined Rutaceous subfamilies mainly based on gynoecial and fruit characters.

Analysis of whole chloroplast genomes from the genera of the Clauseneae, the curry tribe (Rutaceae, Citrus family)

The Clauseneae (Aurantioideae, Rutaceae) is a tribe in the Citrus family that, although economically important as it contains the culinary and medicinally-useful curry tree (Bergera koenigii), has been relatively understudied. Due to the recent significant taxonomic changes made to this tribe, a closer inspection of the genetic relationships among its genera has been warranted. Whole genome skimming was used to generate chloroplast genomes from six species, representing each of the four genera (Bergera, Clausena, Glycosmis, Micromelum) in the Clauseneae tribe plus one closely related outgroup (Merrillia), using the published plastome sequence of Citrus sinensis as a reference. Phylogenetically informative character (PIC) data were analyzed using a genome alignment of the seven species, and variability frequency among the species was recorded for each coding and non-coding region, with the regions of highest variability identified for future phylogenetic studies. Non-coding regions exhibited a higher percentage of variable characters as expected, and the phylogenetic markers ycf1, matK, rpoC2, ndhF, trnS-trnG spacer, and trnH-psbA spacer proved to be among the most variable regions. Other markers that are frequently used in phylogenetic studies, e.g. rps16, atpB-rbcL, rps4-trnT, and trnL-trnF, proved to be far less variable. Phylogenetic analyses of the aligned sequences were conducted using Bayesian inference (MrBayes) and Maximum Likelihood (RAxML), yielding highly supported divisions among the four genera.

Melicope oppenheimeri, section Pelea (Rutaceae), a new species from West Maui, Hawaiian Islands: with notes on its ecology, conservation, and phylogenetic placement

Abstract Melicope oppenheimeri K.R. Wood, Appelhans & W.L. Wagner (section Pelea (A. Gray) Hook. f., Rutaceae), a rare endemic tree from West Maui, Hawaiian Islands, is described and illustrated with notes on its ecology, conservation, and phylogenetic placement. The new species differs from Hawaiian congeners by its carpels basally connate 1/5, narrowed into a strongly reflexed beak 10–15 mm long. It also differs in a combination of leaves with 7–10 pair of secondary veins; cymes to 3 cm long; peduncles 5–6.5 mm long; flowers perfect; capsules 4–9 × 40–52 mm; and a densely appressed short-sericeous ovary. Melicope oppenheimeri is known only from an isolated cliff-base plateau in upper Waihe‘e Valley, West Maui. Its discovery brings the number of recognized Melicope J.R. Forst. & G. Forst. species in the Hawaiian Islands to 49. A table is included indicating the conservation status of Hawaiian Melicope and Platydesma H. Mann., which is nested within Melicope sect. Pelea. Melicope oppenheimeri falls into the IUCN Critically Endangered (CR) Red List category.

Reduction of the Hawaiian genus Platydesma into Melicope section Pelea (Rutaceae) and notes on the monophyly of the section

Abstract Platydesma, an endemic genus to the Hawaiian Islands containing four species, has long been considered of obscure origin. Recent molecular phylogenetic studies have unequivocally placed Platydesma within the widespread genus Melicope as sister to the rest of the Hawaiian species of Melicope. This makes submerging Platydesma into Melicope necessary. We make the necessary new combinations: Melicope cornuta (Hillebr.) Appelhans, K.R. Wood & W.L. Wagner, M. cornuta var. decurrens (B.C.Stone) Appelhans, K.R. Wood & W.L. Wagner, M. remyi (Sherff) Appelhans, K.R. Wood & W.L. Wagner, and M. rostrata (Hillebr.) Appelhans, K.R. Wood & W.L. Wagner. An additional species that has been recognized within Platydesma should now be recognized under its original name M. spathulata A. Gray. All Hawaiian species belong to Melicope section Pelea. Our molecular phylogenetic studies also showed that in addition to merging Platydesma into section Pelea, five species described from New Caledonia need to be excluded from the section in order to achieve monophyly of section Pelea.

Melicope stonei, section Pelea (Rutaceae), a new species from Kaua'i, Hawaiian Islands: with notes on its distribution, ecology, conservation status, and phylogenetic placement.

Abstract Melicope stonei K.R. Wood, Appelhans & W.L. Wagner (section Pelea, Rutaceae), a new endemic tree species from Kaua‘i, Hawaiian Islands, is described and illustrated with notes on its distribution, ecology, conservation status, and phylogenetic placement. The new species differs from its Hawaiian congeners by its unique combination of distinct carpels and ramiflorous inflorescences arising on stems below the leaves; plants monoecious; leaf blades (5–)8–30 × (4–)6–11 cm, with abaxial surface densely tomentose, especially along midribs; and very long petioles of up to 9 cm. Since its discovery in 1988, 94 individuals have been documented and are confined to a 1.5 km2 region of unique high canopy mesic forest. Melicope stonei represents a new Critically Endangered (CR) single island endemic species on Kaua‘i.

Phylogeny of Acronychia (Rutaceae) and First Insights into Its Historical Biogeography and the Evolution of Fruit Characters

Background The genus Acronychia (Citrus family, Rutaceae) contains 49 species of trees and shrubs that are found mainly in rain forest. The genus has a large distributional range from mainland southern Asia to Australia and New Caledonia, but most species are endemic to either New Guinea or Australia. This study aimed to provide the first detailed molecular phylogeny of Acronychia and use it to test the taxonomic value of fruit morphological characters, and infer the historical biogeography of the genus. Methodology Phylogenetic analyses (Bayesian Inference, Maximum Likelihood) were undertaken on nucleotide sequence data from two plastid (psbA-trnH, trnL-trnF) and three nuclear markers (ETS, ITS, NIAi3) from 29 Acronychia species (59% of the genus) and representatives of related genera. Results and Conclusions The results indicate that the South-East Asian genus Maclurodendron is nested phylogenetically within Acronychia and must be synonymized to render Acronychia monophyletic. Fruit morphological characters have been used previously to infer relationships within Acronychia and our analyses show that these characters are informative for some subclades but are homoplasious for the group as a whole. Apocarpous fruits are the ancestral state in Acronychia and subapocarpous and fully syncarpous fruits are derived. The unisexual flowers of Maclurodendron are derived from bisexual flowers, which are found in all species of Acronychia as well as its relatives. Acronychia probably first evolved on Australia with range expansion to New Guinea via stepping-stone dispersal or direct land connections within the Sahul Shelf, followed by two independent dispersals to areas west of New Guinea. Most species of Acronychia occur in either Australia or New Guinea, but no species occurs in both regions. This is surprising given the close proximity of the landmasses, but might be explained by ecological factors.

Phylogeny and biogeography of the pantropical genus Zanthoxylum and its closest relatives in the proto-Rutaceae group (Rutaceae)

Zanthoxylum L. (prickly ash) is the only genus in the Citrus L. family (Rutaceae) with a pantropical distribution. We present the first detailed phylogenetic and biogeographic study of the genus and its close relatives in the proto-Rutaceae group. Our phylogenetic analyses based on two plastid and two nuclear markers show that the genus Toddalia Juss. is nested within Zanthoxylum, that earlier generic and intrageneric classifications need revision, and that the homochlamydeous flowers of the temperate species of Zanthoxylum are the result of a reduction from heterochlamydeous flowers. The biogeographic analyses reveal a Eurasian origin of Zanthoxylum in the Paleocene or Eocene with successive intercontinental or long-range migrations. Zanthoxylum likely crossed the North Atlantic Land Bridges to colonize the Americas in the Eocene, and migrated back to the Old World probably via the Bering Land Bridge in the Oligocene or Miocene. Zanthoxylum also colonized several Pacific Islands and the Hawaiian clade shows phylogenetic incongruence between the plastid and nuclear datasets, suggesting hybridization. The Hawaiian species are one of the rare examples of endemic Hawaiian lineages that are older than the current main islands.

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

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.

On the identity of Blanco's Cissus frutescens and its correct name in Melicope (Rutaceae) with neotypification of Cissus arborea Blanco.

Abstract The names Cissus frutescens and Cissus arborea have a long history of confusion. Cissus frutescens Blanco belongs to the genus Melicope (Rutaceae) and we herein correct a nomenclatural mistake made by T.G. Hartley in the revision of Melicope. The name Melicope confusa (Merr.) P.S. Liu was accepted for this taxon by Hartley. However, Cissus frutescens Blanco represents the earliest name for this entity and a new combination, Melicope frutescens (Blanco) Appelhans & J.Wen is herein proposed. Neotypification of Cissus arborea Blanco is also provided.