Citrus taxonomy


Citrus taxonomy is the botanical classification of the species, varieties, cultivars, and graft hybrids within the genus Citrus and related genera, found in cultivation and in the wild.
Citrus taxonomy is complex and controversial. Cultivated citrus are derived from various citrus species found in the wild. Some are only selections of the original wild types, many others are hybrids between two or more original species, and some are backcrossed hybrids between a hybrid and one of the hybrid's parent species. Citrus plants hybridize easily between species with completely different morphologies, and similar-looking citrus fruits may have quite different ancestries. Some differ only in disease resistance. Conversely, different-looking varieties may be nearly genetically identical, and differ only by a bud mutation.
Genomic analysis of wild and domesticated citrus cultivars has suggested that the progenitor of modern citrus species expanded out of the Himalayan foothills in a rapid radiation that has produced at least 11 wild species in South and East Asia and Australia, with more than a half-dozen additional candidates for which either insufficient characterization prevents definitive species designation, or there is a lack of consensus for their placement within the Citrus genus rather than sister genera. Most commercial cultivars are the product of hybridization among these wild species, with most coming from crosses involving citrons, mandarins and pomelos. Many different phylogenies for the non-hybrid citrus have been proposed, and the phylogeny based on their nuclear genome does not match that derived from their chloroplast DNA, probably a consequence of the rapid initial divergence. Taxonomic terminology is not yet settled.
Most hybrids express different ancestral traits when planted from seeds and can continue a stable lineage only through vegetative propagation. Some hybrids do reproduce true to type via nucellar seeds in a process called apomixis. As such, many hybrid species represent the clonal progeny of a single original F1 cross, though others combine fruit with similar characteristics that have arisen from distinct crosses.

Genetic history

All of the wild 'pure' citrus species trace to a common ancestor that lived in the Himalayan foothills, where a late-Miocene citrus fossil, Citrus linczangensis, has been found. At that time, a lessening of the monsoons and resultant drier climate in the region allowed the citrus ancestor to expand across south and east Asia in a rapid genetic radiation. After the plant crossed the Wallace line, a second radiation took place in the early Pliocene to give rise to the Australian species.
Most modern cultivars are actually hybrids derived from a small number of 'pure' original species. Though hundreds of species names have been assigned, a recent genomic study by Wu et al. identified just ten ancestral species of citrus among more than a hundred cultivars studied. Of these ten, seven were native to Asia:
Three from Australia were identified:
Many other cultivars previously identified as species were found to be closely related variants or hybrids of these species, though not all cultivars were evaluated. Subsequent studies have added two additional species to this list of pure species: a mandarin native to the Ryukyu Islands designated C. ryukyuensis, and a rare wild species from Southeast Asia, the mountain citron. A number of further species originally placed in other genera have recently been subsumed into Citrus as a result of phylogenetic analysis, but these have yet to be characterized on a phylogenomic level to confirm their status as unique pure species.
Artificial interbreeding seems possible among all citrus plants, though there are certain limitations to natural interbreeding due to plant physiology and differences in natural breeding seasons. This ability to cross-pollinate extends to some related species that some classifications place in distinct genera. The ability of citrus hybrids to self-pollinate and to reproduce sexually also helps create new varieties, as does spontaneous mutation and genome duplication. The three most predominant ancestral citrus taxa are citron, pomelo, and mandarin. These taxa interbreed freely, despite being quite genetically distinct, having arisen through allopatric speciation, with citrons evolving in northern Indochina, pomelos in the Malay Archipelago, and mandarins in Vietnam, southern China, and Japan. The hybrids of these taxa include familiar citrus fruits like oranges, grapefruit, lemons, and some limes and tangerines. These three have also been hybridized with other citrus taxa, for example, the Key lime arose from a citron crossing with a micrantha. In many cases, the varieties are propagated asexually, and lose their characteristic traits if bred. Some of the hybrids have in turn interbred with one another hybrid or with the original taxa, making the citrus family tree a complicated network.
Kumquats do not naturally interbreed with core taxa due to different flowering times, but hybrids exist. Australian limes are native to Australia and Papua New Guinea, so they did not naturally interbreed with the core taxa, but they have been crossbred with mandarins and calamansis by modern breeders. Humans have deliberately bred new citrus fruits by propagating seedlings of spontaneous crosses, creating or selecting mutations of hybrids,, and crossing different varieties.

Citrus naming systems

Initially, many citrus types were identified and named by individual taxonomists, resulting in a large number of identified species: 870 by a 1969 count. Some order was brought to citrus taxonomy by two unified classification schemes, those of Chōzaburō Tanaka and Walter Tennyson Swingle, that can be viewed as extreme alternative visions of the genus.
Swingle's system divided the Citrinae subtribe into three groups, the 'primitive citrus' distant relatives, the closer 'near citrus' including citrus-related genera like Atalantia, and the "true citrus", for the species that had historically been placed in Citrus but many of which he elevated to separate genera: Poncirus, Fortunella, Eremocitrus, Microcitrus, as well as an additional genus, Clymenia, formerly thought to be a citrus hybrid. His Citrus he likewise subdivided into two subgenera: citrons, pomelos, mandarins, oranges, grapefruits and lemons were placed in subgenus Eucitrus, while the hardy but slow-growing trees with relatively unpalatable fruit he placed in subgenus Papeda. His genus Citrus consisted of just 16 species, dividing them further into varieties, and lastly cultivars or hybrids. The Swingle system is generally followed globally today with much modification; there are still large differences in nomenclature between countries and individual scientists.
The 'Tanaka system' instead provides a separate species name for each cultivar, regardless of whether it is pure or a hybrid of two or more species or varieties, and resulted in 159 identified species. It thus represents an example of taxonomic "splitting", and in assigning separate species names to horticultural variants does not conform to the standard species concept. Tanaka also divided into subgenera, but different than in Swingle's system, introducing Archicitrus and Metacitrus. This system is commonly used in Tanaka's native Japan. A 1969 analysis by Hodgson intended to harmonize the two schemes accepted 36 species.
These initial attempts at Citrus systematization all predated the recognition, which began to gain traction in the mid-1970s, that the majority of cultivars represent hybrids of just three species, citron, mandarin and pomelo. Phylogenetic analysis confirms this hybrid origin of most citrus cultivars, indicating a small number of founder species. While the subgenera suggested by Tanaka proved similar to the phylogenetic divisions of pure founder species, Swingle's subgenera were polyphyletic, and hence do not represent valid taxonomy. His novel genera also fail to withstand phylogenetic analysis. Swingle had elevated kumquats into a separate genus Fortunella, while two genera were suggested by him for the Australian limes, Microcitrus and Eremocitrus. However, genomic analysis shows these groups nested within the phylogenetic tree of Citrus. Since their placement in distinct genera would make Citrus a paraphyletic grouping, it has been suggested that all of these are correctly members of the genus Citrus. Similarly, genomic analysis has suggested that other genera previously split off from Citrus likewise belong within this expanded phylogenetic concept of the genus Citrus, including Clymenia, Oxanthera and more controversially Poncirus, which is the earliest branching of Swingle's genera, and a genus not previously recognized as a close citrus relative, Feroniella. There remains a lack of consensus as to which wild plants and hybrids merit distinct species status, a phenomenon exacerbated by the prior failure to correctly identify the genetically pure citrus strains and distinguish them from hybrids.
In 2020, a new taxonomic system was proposed by Ollitrault, Curk and Krueger, with the goal of harmonizing traditional naming systems with the new genomic data that have both allowed the pure ancestral species to be distinguished from hybrids, and enabled the ancestry of those hybrids to be identified among the ancestral species. In their system, each ancestral species has a binomial name, while a unique species name is reserved for each combination of ancestral species, independent of the specific order of crossing or proportional representation of the ancestral species in a given hybrid.
Individual hybrids of each type are then distinguished by a variety name. Thus hybrids that are crosses between mandarin and pomelo would all be C. × aurantium, with specific crosses including: C. × aurantium var. sinensis for the sweet orange, C. × aurantium var. paradisi for grapefruit, and C. × aurantium var. clementina for the clementine. Likewise, hybrids combining mandarins and citrons would all be varieties of C. × limonia, those of pomelo and citron, C. x lumia, while tri-species hybrids of citrons, pomelos and mandarins would be C. × limon, and a tetra-species cross involving these three species along with C. micrantha would be C. × latifolia.
This naming system focused on the four species ancestral to most commercial hybrids, and did not include similar species designations for more exotic hybrids involving other citrus species, such as the Ichang papeda, kumquat, or trifoliate orange. Likewise, Ollitrault, Curk and Krueger accepted that the whole-genome characterization necessary to unambiguously assign a hybrid species name under their system is not available for many varieties.