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Review

Understanding the Taxonomic Complexes and Species Delimitation within Sambucus L. (Viburnaceae)

by
Emmanuel Nyongesa Waswa
1,2,3,4,
Elizabeth Syowai Mutinda
1,2,3,4,
Elijah Mbandi Mkala
1,2,3,4,
Daniel Mutavi Katumo
1,2,3,4,
Millicent Akinyi Oulo
1,2,3,4,
Wyclif Ochieng Odago
1,2,3,4,
Sara Getachew Amenu
1,2,3,4,
Shi-Xiong Ding
1,2,3,4 and
Guang-Wan Hu
1,2,3,4,*
1
Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China
2
Center of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Wuhan 430074, China
3
Sino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan 430074, China
4
Wuhan Botanical Garden, Flora and Plant Taxonomy of East Africa, Department of Botany, University of Chinese Academy of Sciences, Beijing 101408, China
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(11), 906; https://doi.org/10.3390/d14110906
Submission received: 26 September 2022 / Revised: 18 October 2022 / Accepted: 22 October 2022 / Published: 26 October 2022
(This article belongs to the Section Plant Diversity)
Browse Figures
Versions Notes

Abstract

:
The genus Sambucus belongs to the family Viburnaceae, and has long been a debatable taxon regarding its systematics and taxonomic assignment. It is known for its morphological and genetic variations and thus the taxonomic delimitation remains uncertain. Phenotypic and genotypic variations within plant species causes difficulties in the detection of species boundaries. In the present review, we compiled a set of studies that assessed species discrimination within Sambucus genus by morphological and molecular markers as well as the taxonomic uncertainties in the re-circumscription of the segregated genera i.e., Viburnum L., Sambucus L., and Adoxa L., (syn. Sinadoxa C.Y. Wu, Z.L. Wu & R.F. Huang/Tetradoxa C.Y. Wu) from Caprifoliaceae and their family assignment. The data was obtained from published journal articles and various online databases. Morphological and molecular diagnostic characters were employed to distinguish Sambucus species. Our findings indicated that high intraspecific variations within narrow-ranged populations and their widespread counterparts contribute to its taxonomic complications. Additionally, intraspecific variations within Sambucus species leads to misidentifications and the misapplication of names, occasioning the publication of many putative synonyms and ambiguous names. Possible interspecific hybridizations experienced between Sambucus species increases complexity in character evolution. A morphological analysis showed that the endocarp seed morphological characters can reliably support the segregation of Sambucus taxa into discrete taxonomic entities. In molecular analysis, the NeighborNet (NN) phylogenetic split network revealed three distinct genera including Viburnum, Sambucus, and Adoxa, which clustered separately. The Maximum Likelihood (ML) analysis indicated that the Sambucus species formed a monophyletic group and clustered into two major clades, a small clade containing S. maderensis, S. peruviana, S. nigra, and S. canadensis, and a large clade encompassing the rest of the species with significantly supported clades (<52%). The preferred family assignment for Sambucus is Viburnaceae.

1. Introduction

Dipsacales (Valerianaceae, Dipsacaceae, Viburnaceae, and Caprifoliaceae sensu lato which includes Linnaeaceae, Diervillaceae, and Caprifoliaceae sensu stricto) and Paracryphiales; Takht. Ex Reveal with a single-family called Paracryphiaceae [1] are the recent angiosperm order that diverged in the mid-Campanian between 82.7 and 78.9 Ma [2]. The family Viburnaceae Raf., a member of Dipsacales, encompass the three accepted genera, Viburnum L., Sambucus L., and Adoxa L. Viburnum is the largest genus with approximately 196 accepted species while Adoxa L., (syn. Sinadoxa C.Y. Wu, Z. L. Wu & R.F. Huang/ Tetradoxa C.Y. Wu) is the smallest with only four accepted species including Adoxa moschatellina, Adoxa corydalifolia (Sinadoxa corydalifolia), Adoxa omeiensis (Tetradoxa omeiensis), and Adoxa xizangensis.
Sambucus L. is a morphologically diverse group of plants that have always been confounded by taxonomists. This genus comprises approximately 23 accepted species that are mostly deciduous shrubs, perennial herbs or small trees widespread in almost all regions of the world excluding the extremely cold and desert zones [3]. They are characterized by compound, pinnate to ovate-lanceolate, or ovate-elliptic with serrated margin leaves (Figure 1). The flowers are born in terminal flat topped umbellate or corymbose cymes that are pyramidal paniculate [4]. The fruits are small rounded berry-like drupes (4–7 mm in diameter) with distinct colors at maturity, three to five pyrenes, and three to five triquetrous or ellipsoid seeds [5,6]. The center of generic diversity is central Asia [7], with the parent type established as long as the Oligocene period. The two distinct routes of Sambucus dispersal cover an area west to Europe, North America, South America, and northern Asia; and east to South east Asia and Australia.
Sambucus species are difficult to be delimitated based solely on morphological characters, thus there is a necessity for taxonomic clarification since the many so-called species are merely horticultural clones [8]. To date, many species complexes remain unclear with little consensus on the number of species and infraspecific taxonomic ranks.

2. Materials and Methods

The present work is based on extensive scrutiny and analysis of relevant literatures and online databases. The databases that facilitated our study include Google Scholar, Web of Science, Science Direct, and PubMed, with the single or combination of keywords; Adoxaceae, Sambucus delimitation, endocarps, hybridizations, morphology, and taxonomy without specific limit.

2.1. Taxonomic and Nomenclatural Complexes

A literature search was conducted to compile representative views of studies on the taxonomic, nomenclatural treatments and taxa discrimination within the Sambucus genus. Comprehensive searches for published articles were conducted with no restrictions on the language or quality of publications. The taxonomic and nomenclatural datasets on various taxa were obtained from the World Flora Online (http://www.worldfloraonline.org/ accessed on 13 July 2022), Plants Of the World Online (https://powo.science.kew.org/ accessed on accessed on 13 July 2022), International Plant Names Index (https://www.ipni.org/ accessed on 13 July 2022), and Global Biodiversity Information Facility (http://www.worldfloraonline.org accessed on 13 July 2022).

2.2. Morphological Data

The endocarp morphological datasets (Table 1), used for preliminary analysis were retrieved from published sources, including Bojnanský & Fargašová [9], Jacobs et al., [10], and Huang et al. [11] journal articles. The cluster analysis of the obtained morphological characters was performed to confirm their morphological affinities using Mesquite software v.3.04 [12].

2.3. Molecular Data

In the molecular analysis, the Internal transcribed spacers (ITS) dataset from Viburnum (DQ005993, DQ005992); Sambucus (AH006915, DQ009613, U88195, U41381, U88196, DQ521255, AY265157, U88199, U88200, DQ521256, U41382, U88201, U88202, U88204, U88205, U88207, AY236171, U88559, U88208), and Adoxa (U88194, AF248611, AJ419710) were downloaded from National Center of Biotechnology Information (NCBI) (https://www.ncbi.nlm.nih.gov/ accessed on 29 July 2022). They were used to assess the robust phylogenetic relationships within Sambucus genus by the Maximum Likelihood (ML) method using Phylosuite software (http://phylosuite.jushengwu.com/ accessed on 30 July 2022) based on 5000 replicates with a single search replicate per bootstrap replicate. The distance-based network construction method, NeighborNet (NN) incorporated in the SplitsTree4 v.4.14.4 (www.splitstree.org accessed on 3 August 2022) was used to reconstruct phylogenetic split networks. The results were compared with those previously obtained by Eriksson & Donoghue [13].

3. Results

3.1. Taxonomic Complexes within Sambucus

The morphological species concept describes species based on phenotypic or anatomical characteristics. Species are the smallest groups that are consistently distinct and distinguishable [14]. Nevertheless, the characteristics that lead to this subjective judgment are often unclear, sometimes even to taxonomic experts [8]. The species concept may become subjective at times, particularly when there is a mismatch between morphospecies and genetic lineages [15]. The perspectives on morphological classification are frequently biased based on researcher preferences or weighting characteristics. For instance, when characters of special value are weighed, most taxonomists’ focus is always inclined towards reproductive rather than vegetative characters. Since the methods used by taxonomists are not always evident, they may lead to some conflicting taxonomic treatments that are based on taxonomists’ reputations rather than inherent qualities of classification. The taxonomy of Sambucus is challenging due to plastic morphological characters within and between species as well as great variability between their widespread congeners [3]. Most Sambucus species show genetic diversity within their populations. Existence of a geographical pattern leads to intraspecific variation since the disparity is usually non-random throughout the range occupied by the species. Although there might be intraspecific variations, there exists a clear discontinuity between members of different species. Widespread Sambucus species typically exhibit greater genetic and phenotypic diversity than their narrow-ranged counterparts, resulting in unclear boundaries between some species.
Von Schwerin [16] in his taxonomic work which relied heavily on important diagnostic morphological characters, recognized 28 Sambucus species and several varieties. Bolli [7] submerged nine species in the Sambucus genus to subspecific rank, while several others were synonymized. The species S. canadensis, S. cerulea, S. peruviana, S. maderensis, and S. palmensis were regarded as subspecies of S. nigra, whereas S. koreana, S. miquelii, S. sibirica, and S. tigranii were considered to be subspecies of S. racemosa. Bolli’s phylogeny was simplified by placing more emphasis on morphological similarities within the group, which was heavily influenced by general discussions of character evolution and trends. Nine species; S. ebulus L., S. wightiana Wall. Ex Wight et Arnott, S. adnata DC., S. gaudichaudiana DC., S. australasica (Lindley) Fritsch, S. javanica Blume, S. nigra L., S. australis Cham. Et Schlecht. And S. dnatee L. were reputed to be part of this genus. Conversely, no molecular data were used to support this drastic submersion of species to infraspecific ranks.
Presently, the Sambucus genus encompasses about 37 accepted names including 23 species, six subspecies, six varieties, and two forms (https://powo.science.kew.org, accessed on 30 August 2022). Interestingly, the genus has the highest number of synonyms (52%) and unresolved names (34%), while accepted names are the least (14%) (Figure 2). In total, 143 synonyms and 91 ambiguous names are recognized in Sambucus genus (http://www.worldfloraonline.org, accessed on 30 August 2022).

3.2. Morphological Species Delimitation in Sambucus

Morphospecies are typically circumscribed based on morphological characters that are seemingly fixed and diagnostic (invariant within the putative species or are at least non-overlapping) to distinguish them from others. Character fixation is a common criterion in morphological species delimitation. Traditionally, problematic taxa were assigned into groups based on a few or even a single character weighted principally on priori grounds [17]. However, morphological species discrimination is time-consuming and requires a high level of expertise [18].
Several morphological diagnostic features based on preliminary data i.e., habit, rhizome, inflorescence form, fruit mesocarp color when ripe, corolla lobe apex, and pith color were used to infer phylogenetic relationships among Sambucus species [13]. In this investigation, the red-fruited species S. sieboldiana, S. racemosa, S. pubens, S. callicarpa exhibited paniculate inflorescences, reddish-brown pith color, and buds with preformed inflorescence and formed a clade with S. melanocarpa, a black-fruited species. Additionally, the valvate corolla lobes united S. javanica, S. adnata, S. ebulus, S. africana, and S. wightiana into a single monophyletic clade. However, several phylogenetically separate lines exist within these groups, and additional characters are required to establish major boundaries within the Sambucus taxa [10,19].

Palynological and Endocarp Characters

Pollen morphology is significant in paleobotany, phylogeny, and taxonomic purposes. It acts as valuable backing in delimiting ambiguous taxonomic entities at the genus and species levels [20]. In the previous investigation, pollen diagnosis distinguished S. nigra, S. canadensis, and S. williamsii as discrete taxonomic taxa [5]. However, pollen grains of S. nigra and S. ebulus were closely related with respect to size and shape, whereas that of S. racemosa differs in size and proximale/equatorial ratio [20]. Pollen can be applied as supporting evidence to justify the recognition of morphologically distinct species, but are similar enough to be of uncertain status. Nevertheless, taxon circumscription cannot be achieved when pollen alone is used as a practical key for species assignment and delimitation since the morphological pollen differentiation in the Sambucus species is quite low [11]. Thus, pollen tends to be an unreliable source of data to discriminate the Sambucus species. The pollen characters are rarely used in revisionary studies mostly because they cannot be observed either in the field with a hand lens or in the herbarium with a dissecting microscope [8].
The endocarp is the innermost layer of the pericarp surrounding a seed. Sambucus endocarps are usually variable in shape, size, and surface characteristics [10]. The earliest known Sambucus fossil endocarp was found in Southern England during the Palaeocene period [21]. They were also recorded in Europe [22], northeastern Asia [23], and northern North America [24] from the Paleocene to the Holocene. The fossil endocarps found in Europe, Siberia, and Southwest China are within their modern distribution regions while those from northern North America are out of their modern distribution regions [11]. This implies that they might have been living at higher latitudes in the geological past than they are at present.
The morphology of Sambucus seeds endocarps are of taxonomic significance and provide highly reliable diagnostic features for species identification [25]. Most Sambucus species employed in the present study exhibited different morphological profiles based on the seven morphological markers employed (Table 2). Sambucus species are highly distinguished by the bases, sizes, length-width ratio, number of ridges, and surface details of endocarps. The majority of Sambucus seed endocarps are characterized by a roundish apex, whereas in S. canadensis they are nearly straight, and they remain unknown in S. australis. Sambucus pubens, S. racemosa, S. williamsii, S. mexicana, and S. alveolatisemina have either roundish or slightly roundish bases, whereas almost all of the endocarps of the remaining species are gradually narrowed [9,10,11].
The discrimination of Sambucus species based on qualitative and quantitative traits of seed endocarps and the extent of similarities between them are presented in Figure 3. Seed endocarps can thus be used as supporting characters to separate the Sambucus taxa into distinct species because they provide a key for species identification [10,19]. However, the existence of only a few morphological differences between the closely related taxa does not satisfactorily elucidate their species status.

3.3. Molecular Species Delimitation in Sambucus

Molecular-based methods provide new insights and opportunities for clear species delimitation [26]. The molecular ITS dataset showed precise separation of the genera within Viburnaceae, comparable to the results obtained by Eriksson & Donoghue [13]. Three distinct genera including Viburnum, Sambucus, and Adoxa were recovered in the NeighborNet (NN) phylogenetic split networks and the Maximum Likelihood (ML) analyses (Figure 4a,b). The results obtained by both methods showed remarkable similarities with slight variations in the clustering of species. Adoxa, the smallest genus, is closely related to Sambucus. Adoxa, Sinadoxa, and Tetradoxa clustered together and displayed a sister relationship, congruent to previous findings [10]. In the present study, we treated Sinadoxa C.Y. Wu, Z.L. Wu & R.F. Huang and Tetradoxa C.Y. Wu as synonyms of Adoxa L (https://powo.science.kew.org/ accessed on 13 July 2022). The ML analysis suggested that the Sambucus species formed a monophyletic group and clustered into two major clades, a small clade containing S. maderensis, S. peruviana, S. nigra, and S. canadensis, and a large clade encompassing the rest of the species with significant bootstrap support values (<52%). In the larger clade, the closely related S. adnata, S. javanica, and S. wightiana formed a sister branch with S. cerulea.
Several phylogenetically separate lines exist within the Sambucus genus, comparable with the clustering of endocarp morphological characters with slight topological variations (Figure 3 and Figure 4). Sambucus racemosa, S. sieboldiana, S. cerulea, S. wightiana, S. javanica, and S. adnata form a clade related to S. australis. The species S. adnata and S. javanica are closely related (Figure 4b), with high morphological similarities (http://www.worldfloraonline.org/ accessed on 13 July 2022). Additionally, S. wightiana is highly similar to the latter, but differs with its large stipules. Sambucus maderensis, S. nigra, S. peruviana, S. nigra, and S. canadensis clustered in the same clade and are related to the rest of the Sambucus species.
Incomplete reproductive isolation among the closely related species can lead to hybridization. This may result in faster introgression of maternally inherited chloroplast DNA (cpDNA) fragments and high evolution of the nuclear genes, which could distort their phylogenetic relationships [27]. An investigation using polymorphic microsatellite markers showed that different natural populations of Sambucus palmensis Link. exhibited considerably high genetic variations among and within populations [28]. The long geographically-isolated populations accumulated private alleles causing significant genetic differentiation. Examination of Sambucus phylogenetic relationships using ITS sequences by Eriksson & Donoghue [13] showed S. javanica, S. adnata, S. ebulus, S. africana and S. wightiana groups and sects. The Botryosambucus clade, which encompassed the recognized subspecies of S. nigra by Bolli [7], except S. cerulea, was monophyletic. In this clade, S. nigra clustered with S. canadensis, S. maderensis, and S. peruviana, and thus were in the same clade, while S. cerulea clustered into a separated clade and was treated as an independent species. An investigation by simple sequence repeats showed that the primers of S. canadensis consistently amplified products that were generally distinct from the primers amplified by S. nigra [29], supporting the discrimination and recognition of S. nigra and S. canadensis as distinct taxonomic entities. However, minor morphological characters were found to separate S. peruviana, S. maderensis, and S. palmensis from S. nigra, similar to S. koreana, S. miquelii, S. sibirica, and S. tigranii from S. racemosa [7], necessitating further molecular investigations to confirm their taxonomic treatment. Generally, only a few molecular studies have been performed to discriminate Sambucus species [7,13,28], and thus more molecular studies are required.

3.4. Interspecific Breeding Potential

The interbreeding species concept focuses almost entirely on the ability of species to naturally or artificially transfer genes. High intraspecific variation may cause complications in taxon identification [30]. Geographically widespread species exhibit greater genetic and phenotypic variability than their endemic congeners [8]. Additionally, the populations of a species in a given area tends to show uncertain boundaries due to possible intraspecific variations triggering complexity in character evolution. Hybridization often occurs among the closely related species with incomplete reproductive isolations [27]. This may cause introgression, the formation of new species, or the emergence of sterile offspring [31]. Interspecific-induced hybridization enhances unidirectional improvement or selection of the desired traits. Species complexes within the genus whose members overlap morphologically will cross easily, and are usually noticeable in a group of species whose boundaries are arbitrary and are separated by a few characters that are often correlated with different geographic regions. This phenomenon has been experienced in the Sambucus genus. For instance, the interspecific hybridization concerning S. nigra and S. canadensis were successful, and some of their progenies were sterile [32].
Several interspecific hybridizations between Sambucus species including S. canadensis × S. cerulea [33], S. canadensis ×S. pubens Michx, [34], S. nigra × S. ebulus and S. nigra × S. racemosa [35], S. canadensis × S. nigra, and S. cerulea × S. nigra [36] in the earliest systematics were aimed to produce hybrid plants. A reciprocal cross between S. racemosa and S. nigra produced fruits but their seeds were not viable, hence they were unable to germinate. The cross between S. nigra and S. ebulus produced four hybrid plants while the reciprocal cross produced seeds with no progeny [35]. Additionally, several crosses between S. canadensis and S. nigra produced seeds but very few seedlings in one set, whereas production seeds with no seedlings were revealed in the next set, and the last set was sterile. Alternatively, the cross between S. cerulea and S. nigra produced both seeds and seedlings [36], indicating possible hybridizations between Sambucus species which may highly affect the species delimitation process. A high fertility level was achieved when the closely related species, i.e., S. nigra × S. canadensis were hybridized, whereas low rates of successful fertilizations were experienced in distantly related species, such as the cross between S. nigra and S. ebulus [3]. Positive interspecific hybridizations in the Sambucus genus are favored by characters such as the same chromosome numbers and similarities in nuclear DNA content.

3.5. Taxonomic Implications in the Sambucus delimitation

The typological description of species by some taxonomists which ignores intraspecific variation and morphological plasticity may cause misinterpretation of individual variants as new specific entities causing over splitting [37]. The taxonomy of the Sambucus genus is complicated due to morphological plasticity between and within species with variable geographical ranges [38]. In this genus, populations within the narrow-ranged species exhibit morphological variations. Additionally, intraspecific variations exist within the species confined at a given geographical area and their widespread counterparts due to genetic isolation by distance [28]. Consequently, they are prone to misidentifications and misapplication of names [8], resulting in the publication of many putative synonyms and ambiguous names (https://powo.science.kew.org/ accessed on 3 August 2022) (Figure 2 and Figure 5). Sambucus canadensis and S. nigra have been highly synonymized whereas S. australis and S. palmensis are the least synonymized species (Figure 4). It remains uncertain whether the 93 reported names in the genus Sambucus (http://www.worldfloraonline.org/ accessed on 3 August 2022), refer to distinct species, infraspecific taxa, or synonymies of other species. Even though the names that authors put in synonymy are not regarded as the correct ones, their establishment represents a synthesis of our knowledge in the taxonomy of plants because a substantial amount of information may be documented in the literature under one or more of these names.
Sambucus javanica Lindl. and S. adnata Blume. are considered as distinct species. However, they share a high degree of morphological similarities united by valvate corolla lobes, yellow anthers, bladelike stipules, umbellate cymes, 3-lobed stigma, urceolate calyx [13,39], among others (Figure 6). Nevertheless, S. javanica is discriminated from the latter by their inconspicuous stem lenticels, connate filaments at the base, and verrucate pyrene fruits (http://www.efloras.org/ accessed on 3 August 2022). Sambucus javanica also differs from S. adnata by its roots that are non-red (vs. red), with the presence of staminate and pistillate (vs. absence of staminate and pistillate) flowers. These species are endemic in China abundantly at the mountain slopes, grasslands, riverfronts, and forests of Gansu, Guizhou, Hubei, Yunnan, Shaanxi, and Sichuan areas and comparably shows limited phenotypic variations. Sambucus chinensis Lindl. is treated as conspecific to S. javanica. Conversely, S. javanica differs from the latter by its red colour of mature fruits. Several studies have reported the intraspecific variations within S. javanica [39,40]. The fruits of Sambucus chinensis were reported by Ohashi [40] to have variable colours, as either blackish purple or red and thus was treated as a form of S. javanica (reddish purple) [39]. The fruits of Sambucus species are usually variable in colours, and are normally recorded as a distinct species in the rank of form [40]. Hu et al., [41] designated a lectotype of S. chinensis Lindl., which sometimes have been viewed as conspecific to S. javanica.
Interbreeding has been experienced in the genus Sambucus resulting in successful hybridizations, and thus the lines within some distinctive species and infraspecific categories are complex. The phenotypic variations within Sambucus species are limited, especially when considering traits associated with fruits and inflorescences, and thus establishing relationships among their major lines requires additional morphological characters [13]. The morphological trait-based classification system in this genus is undependable and controversial, and the outcomes cannot be adopted outright, necessitating molecular-based studies to confirm the taxonomic treatments of taxa.

3.6. Family Assignment of the Genus Sambucus

Nomenclatural type (typus) refers to an element to which the name of a taxon is permanently attached, whether as the correct name or a synonym [42]. However, it is not necessarily the most typical or representative element of a taxon. The typification process entails indicating or designating a type. The family Viburnaceae entails the following typification: (a) Viburnaceae Raf., Annales Generales des Sciences Physiques 6: 87 (1820), nom. cons. Type: Viburnum L. (b) Sambucaceae Batsch ex Borkh., Botanisches Worterbuch 2: 322 (1797). Type: Sambucus L. (c) Adoxaceae E. Mey., Preussens Pflanzengattungen 198 (1839), nom. cons. Type: Adoxa L., nom. cons. [43].
The taxonomy of Viburnaceae (syn. Adoxaceae) has long been confused. The assignment of a family name to the segregated genera i.e., Viburnum L., Sambucus L., and Adoxa L., (syn. Sinadoxa C.Y. Wu, Z.L. Wu & R.F. Huang/Tetradoxa C.Y. Wu) (https://powo.science.kew.org/ accessed on 13 July 2022), from Caprifoliaceae was instigated by molecular studies which necessitated its recircumscription [44,45]. However, the process of excluding the latter from Caprifoliaceae was faced with many discrepancies in the correct family name of the combined genera. The possible ways to be adopted upon removing the above genera from Caprifoliaceae could involve placing each genus into independent segregated families (Sambucaceae, Viburnaceae, and Adoxaceae) or by placing all three genera into a single family.
A proposal to conserve the name Viburnaceae was made to the Nomenclature Committee for Vascular Plants [46]. Following this proposal, if a single-family name is adopted between Sambucaceae, Viburnaceae, and Adoxaceae, Viburnaceae will be the preferred family assignment. However, Reveal, [46] found out that there exists an obsolete family name, Tinaceae Martinov (based on the genus Tinus), a synonym of Viburnum, which was slightly older than Viburnaceae. Proposing to conserve Tinaceae would replace the earlier proposed name “Viburnaceae,” if a single-family classification was adopted. The name Tinaceae had rarely been used before, and adopting it could be confusing to those who preferred using the three-family name classification based on the Linnaean genera. Additionally, more confusion would arise because the name might be presumed to be based on Tina Schult., which is in current use. Having felt that the proposal to adopt Tinaceae would have an undesirable change, Reveal [46] made two more proposals. The first proposal was to “super-conserve” Adoxaceae when Viburnum is united with Adoxaceae and Sambucus, making Adoxaceae the correct family name. The second alternative proposal was to conserve Sambucaceae when Adoxaceae, Viburnum, and Sambucus are united, automatically making Sambucaceae the preferred family name. All the above proposals became the subject of considerable disagreements among members of the Committee and were neither recommended nor rejected by the Specialist Committee since more discussions were needed.
The Nomenclature Committee for Vascular Plants (NCVP) at the Shenzhen International Botanical Congress approved the proposal by Reveal [46] to conserve the name Viburnaceae [47]. This outcome was contrary to the intention of the proposal by Reveal, which aimed at maintaining the nomenclatural stability by making a “super-conservation” proposal on the name Adoxaceae to make it the correct family name since it has been highly used. His “super-conservation” proposal was driven by the fact that the family name Adoxaceae has been overly used. Similarly, the Angiosperm Phylogeny Group III [48] had already favoured the name Adoxaceae by recommending all the involved genera (Adoxa L., Sambucus L., and Viburnum L.) be placed within Adoxaceae, which triggered the overwhelming usage in the past few years, increasing its popularity. Furthermore, the ICN Rec. 14A.1 recommended the existing usage to be adopted.
If the “super-conservation” proposal of the name Adoxaceae was to be rejected, the need to deliberate on whether to reject or adopt Sambucaceae as the correct family name by the committee was required. Adoption of a proposal to conserve Sambucaceae coupled with the rejection of the “super-conservation” proposal of Adoxaceae would allow the above priority to prevail, and the broadly defined family would be called Sambucaceae. Finally, should the committee wish Viburnaceae to be the name for the broadly defined family, then rejection of both proposals to “super-conserve” and to conserve Adoxaceae and Sambucaceae respectively would accomplish that goal.
In August 2016, a proposal report by the general committee to “super-conserve” Adoxaceae against Viburnaceae [49], was reported without recommendation by the NCVP. This was occasioned after two rounds of inconclusive voting without reaching a super-majority, necessitating more discussions. However, the committee voted not to conserve Sambucaceae before a final decision to “super-conserve” Adoxaceae. Later, the Committee rejected the proposal to “super-conserve” Adoxaceae, nom. cons.; thus, the preferred name for the combined genera is Viburnaceae, nom. Cons [50]. Therefore, Viburnaceae is the combined family name of (Adoxa L., Sambucus L., and Viburnum L.), since it was prioritized over the name Adoxaceae.

4. Conclusion and Perspectives

In the present review, we examined the taxonomic complexes within the genus Sambucus. Our findings indicated that the endocarp micromorphology in conjunction with other observable features provided reliable taxonomic resolution in the delimitation of the Sambucus taxa. In addition, the enormous intraspecific variations caused by high genetic diversity that exist within this genus results in taxonomic complications. Defining major boundaries between the Sambucus species and their infraspecific taxa is problematic due to possible hybridizations and morphological plasticity. Intraspecific variations within Sambucus leads to misidentifications and the misapplication of names, resulting in the publication of many putative synonyms and ambiguous names.
The Viburnum, Sambucus, and Adoxa genera are distinct in both the NeighborNet (NN) phylogenetic split network and Maximum Likelihood (ML) analyses. The latter showed that the Sambucus species formed a monophyletic group, and S. adnata, was closely related to S. javanica and S. wightiana. The preferred family assignment of the recognized genera i.e., Viburnum L., Sambucus L., and Adoxa L., (syn. Sinadoxa C.Y. Wu, Z.L. Wu & R.F. Huang/Tetradoxa C.Y. Wu) is Viburnaceae.
Genetic diversity within Sambucus populations creates a wide genetic base, thus recognition of infraspecific taxa should be done with caution in order to simplify classification and prevent confusion. In addition, the re-ranking or “lumping” of infraspecific categories in some cases might enable more accurate species delimitation. An integrative approach and comprehensive sampling are needed to relieve taxonomic complications and bring consistency and clarity across the genus. Thus, we recommend further studies on the structure of seed endocarps and molecular traits to improve the systematics of the Sambucus genus.

Author Contributions

Conceptualization, G.-W.H. and E.N.W.; writing—original draft preparation, E.N.W.; review and editing, M.A.O., D.M.K., E.S.M., E.M.M., W.O.O., and S.-X.D.; grammar, S.G.A.; funding acquisition, G.-W.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (31961143026, 31970211), the National Science & Technology Fundamental Resources Investigation Program of China (2019FY101800), the International Partnership Program of the Chinese Academy of Sciences (151853KYSB20190027) and Sino-Africa Joint Research Center, CAS (SAJC202101).

Acknowledgments

The authors would like to acknowledge Felix Wambua Muema of the Plant Chemical Biology laboratory, Wuhan Botanical Garden for assisting in the editing and improvement of the manuscript.

Conflicts of Interest

The authors declare that they have no conflict of interest.

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Figure 1. Morphological characters of Sambucus species (1). S. adnate Wall. Ex DC (2). S. javanica Blume. (3). S. nigra (a). compound odd-pinnate leaves with serrated margins (b). polychasial cyme, flat-topped inflorescence (c). small rounded berry-like drupes.
Figure 1. Morphological characters of Sambucus species (1). S. adnate Wall. Ex DC (2). S. javanica Blume. (3). S. nigra (a). compound odd-pinnate leaves with serrated margins (b). polychasial cyme, flat-topped inflorescence (c). small rounded berry-like drupes.
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Figure 2. Taxonomic status in the Sambucus genus.
Figure 2. Taxonomic status in the Sambucus genus.
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Figure 3. Cluster analysis of endocarp (seed) morphological traits of Sambucus species.
Figure 3. Cluster analysis of endocarp (seed) morphological traits of Sambucus species.
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Figure 4. Phylogenetic relationship of the accepted Sambucus species inferred by NeighborNet (NN) split network and Maximum Likelihood (ML) based on ITS dataset.
Figure 4. Phylogenetic relationship of the accepted Sambucus species inferred by NeighborNet (NN) split network and Maximum Likelihood (ML) based on ITS dataset.
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Figure 5. Synonymizations of Sambucus species.
Figure 5. Synonymizations of Sambucus species.
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Figure 6. Morphological similarities of S. adnata Wall. ex DC and S. javanica Blume. (a). Red fruits of S. adnata. (b). White flowers of S. javanica.
Figure 6. Morphological similarities of S. adnata Wall. ex DC and S. javanica Blume. (a). Red fruits of S. adnata. (b). White flowers of S. javanica.
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Table
Table 1. Morphological dataset of the Sambucus species.
Table 1. Morphological dataset of the Sambucus species.
SpeciesShapeApexBaseSize (LXW)mmL/WNo. of RidgesSurface Details
S. ebulus000?2-0
S. australis---?1--
S. cerulea111?010
S. canadensis121?111
S. adnata212?102
S. javanica311?103
S. nigra413?114
S. pubens514?123
S. racemosa015?115
S. sieboldiana510?125
S. williamsii615?016
S. alveolatisemina214?117
S. mexicana315?005
All morphological characters are treated as unordered, and different characters of each species is coded with ordered numerical numbers; a dash “-” indicates unknown characters, whereas a question-mark “?”, denotes ambiguous character states. See Table 2 for the list of characters and character states.
Table
Table 2. Endocarp morphological characters in Sambucus species.
Table 2. Endocarp morphological characters in Sambucus species.
SpeciesShapeApexBaseSize (LXW)mmL/WNo. of ridgesSurface details
S. ebulusEllipticSlightly roundishGradually narrowed3.2–3.4 × 1.6–1.81.9–2.0UnknownTransversely ridged
S. australisUnknownUnknownUnknown2.9–3.3 × 1.6–2.01.8UnknownUnknown
S. ceruleaTriangularRoundishNarrowed2.8–3.0 × 1.9–2.11.413–15Transversely ridged.
S. canadensisTriangularNearly straightNarrowed2.6–3.0 × 1.4–1.81.712–15Loosely transversely ridged
S. adnataEllipticRoundishSlightly Narrowed2.3–2.7 × 1.4–1.71.5–1.68–10Transversely ridged, ridge surface
S. javanicaOvate, nearly roundishRoundishNarrowed2.2–2.6 × 1.8–2.21.5–1.67–8Transversely ridged, ridge surface tuberculate
S. nigraOblong ellipticRoundishGradually narrowed with a protuberance2.3–2.7 × 1.3–1.41.7–2.010–11Transversely ridged, ridge surface reticulate and alveolate
S. pubensOblong ellipticRoundishSlightly roundish, gradually narrowed2.0–2.4 × 1.2–1.41.6–1.715–16Transversely ridged, ridge surface tuberculate
S. racemosaEllipticRoundishRoundish2.0–2.3 × 1.2–1.41.6–1.713–14Transverse and weak ridges, ridge surface nearly smooth
S. sieboldianaOblong ellipticRoundishGradually narrowed2.7–3.0 × 1.4–1.61.8–1.917–19Transversely ridged, ridge surface weakly reticulate
S. williamsiiNearly roundishRoundishRoundish2.6–2.9 × 2.2–2.51.1–1.211–13Transversely ridged, ridge surface reticulate, and alveolate
S. alveolatiseminaEllipticRoundishSlightly roundish, gradually narrowed2.1–2.5 × 1.2–1.71.5–1.812–14Transversely and sinuously furrowed
S. mexicanaOvate, nearly roundishRoundishRoundish2.6–2.9 × 1.9–2.11.3–1.49–10Transversely ridged, ridge surface weakly reticulate
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Waswa, E.N.; Mutinda, E.S.; Mkala, E.M.; Katumo, D.M.; Oulo, M.A.; Odago, W.O.; Amenu, S.G.; Ding, S.-X.; Hu, G.-W. Understanding the Taxonomic Complexes and Species Delimitation within Sambucus L. (Viburnaceae). Diversity 2022, 14, 906. https://doi.org/10.3390/d14110906

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Waswa EN, Mutinda ES, Mkala EM, Katumo DM, Oulo MA, Odago WO, Amenu SG, Ding S-X, Hu G-W. Understanding the Taxonomic Complexes and Species Delimitation within Sambucus L. (Viburnaceae). Diversity. 2022; 14(11):906. https://doi.org/10.3390/d14110906

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Waswa, Emmanuel Nyongesa, Elizabeth Syowai Mutinda, Elijah Mbandi Mkala, Daniel Mutavi Katumo, Millicent Akinyi Oulo, Wyclif Ochieng Odago, Sara Getachew Amenu, Shi-Xiong Ding, and Guang-Wan Hu. 2022. "Understanding the Taxonomic Complexes and Species Delimitation within Sambucus L. (Viburnaceae)" Diversity 14, no. 11: 906. https://doi.org/10.3390/d14110906

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