Solanum insanum L. (Solanaceae): Linnaean species or introgressed hybrid? John Samuels Novel Solanaceae Crops Project, Penzance, Cornwall, United Kingdom [email protected] Abstract Wild and weedy forms of brinjal, Solanum melongena L., have historically been referred to as S. insanum L. Views on the precise nature of S. insanum have diverged and its relationship to other wild and weedy brinjal relatives, as well as to brinjal itself, has remained unclear. Opinions have varied as to whether S. insanum populations arise as a result of S. melongena becoming feral, or as a result of hybridisation which may become introgressive. It is suggested here that some S. insanum populations result from hybrid swarms based on reticulate webs of hybridisation and introgression amongst brinjal and sympatric wild relatives. In addition, the correct application of S. insanum L. has proven doubtful and confusing, particularly since the 1980s. As a consequence, consensus on an accepted species concept seems unlikely. Its taxonomic currency is therefore uncertain. Keywords: brinjal eggplant, hybridisation, introgression, Solanum insanum, species concept, weedy, wild relatives 1. Introduction Cultivated brinjal eggplant, or brinjal, (Solanum melongena L.) is economically important in many parts of Asia and elsewhere. Associated with the domesticated forms of this cultigen are wild and weedy forms of South and South-east Asia (sometimes called S. insanum L., S. cumingii Dunal, S. undatum Lam., etc.) and wild relatives in Africa, the Middle East and South Asia (S. campylacanthum Hochst. ex A. Rich., S. lichtensteinii Willd. and S. incanum L.). Together, these taxa are known as the brinjal eggplant complex [1]. Solanum insanum (“wild brinjal”) and S. incanum are considered to be components of the primary genepool of S. melongena. Detailed knowledge of the taxonomic relationships within this group is crucial to our understanding of the origins and domestication of brinjal, and may help in the search for pre-domestication traits that could be useful in crop improvement programmes. 2. The Linnaean concept of S. insanum In the Linnaean protologue S. melongena was originally described [2] as having a prickly calyx. There is no other reference to the presence of prickles elsewhere on the plant, but the stem is described as unarmed. In the Systema Naturae, published by Linnaeus [3] it was placed in the Inermia group, indicating that he subsequently considered it to be completely unarmed, whilst S. insanum was included as a closely related but new species in the Aculeata (“prickly”) group. Also in 1767, the Mantissa Plantarum [4] provided the protologue for S. insanum, describing it as a sparsely prickly annual, morphologically similar to S. melongena by way of its “scarcely-branched stems, stellate tomentum, subsinuate leaves” and “solitary, single- flowered peduncles” producing “large fruits” (see Table 1). Confusingly, the specific epithet insanum was based on the pre-Linnaean name for brinjal: mala insana, the “mad apple.” 129 Solanum insanum was clearly considered to be a close ally of brinjal, but to differ from it by the presence of prickles: “stem with sparse prickles; prickles on both sides of the leaves; calyx very prickly” [4]. The lectotype specimen (sheet 248.29 at LINN-http://linnean- online.org/2605/) designated by Hepper and Jaeger [5] conforms to Linnaeus’ protologue in terms of branching, tomentum and leaf characters; however, the presence of an inflorescence bearing three flowers (rather than one, as described in the protologue) does not conform. Unfortunately, there are no fruits present on the specimen. Thus, the designated lectotype may be an unreliable representation of Linnaeus’ concept of S. insanum. Armature characteristics are highly variable in members of the brinjal eggplant complex [6] and, although cultivated S. melongena may or may not be prickly [7, 8], Linnaeus’ emphasis on prickles as a major diagnostic character seems to have contributed strongly to the taxonomic rationale of delimiting S. insanum from S. melongena. Figure 1: S. insanum: straggly form, Taiwan 3. Varying species concepts The taxonomic proximity of S. insanum and S. melongena suggested by Linnaeus has been recognised and accepted ever since the eighteenth century, but views on the precise nature of S. insanum began to diverge from the 1980s onwards, when crop improvement research became focused on brinjal and its allies (see Table 1). For example, Deb [9] held the opinion that the wild species S. incanum and S. insanum were conspecific (Table 1). This was refuted by Lester and Hasan [10], who showed experimentally that the two were reproductively and morphologically distinct. Deb’s views were supported only by observations in the field; weedy forms of S. melongena also seem to have been mistaken for populations of S. incanum, as the latter never produces the white fruits described by him. Later, Meyer et al. [11] designated the weedy forms from India as “Asian S. incanum” (Table 1), challenging the species concepts of both S. incanum and S. insanum [12, 13]. Recent circumscription of S. incanum [14] refers to characteristics such as inflorescences with up to 15 flowers, and confirms that it is clearly distinct from S. insanum L. sensu stricto, which has single-flowered inflorescences [4]. 130 The concept of S. insanum sensu Lester and Hasan (=S. melongena group E) [7, 10, 15] revolved around the assumption that it was a purely Indian form of S. melongena, with a low- growing, straggly habit, dense armature, and 5-9 flowered inflorescences producing few, smallish, spherical fruits (Table 1). Prain’s [16] view that S. insanum (as S. melongena var. insana [L.] Prain) was a feral, secondary weedy form of S. melongena was supported by Lester and Hasan. Their view of the application of S. insanum L. was adopted as a result of observations of a limited number of accessions collected from northern India, and they reserved judgement as to its correct taxonomic status and nomenclature. There is no indication of growth habit in Linnaeus’ original description of S. insanum, although it is described as “herbaceous,” meaning that plants may be prone to become straggly. The limited material of the lectotype specimen shows no indication of habit, although the single shoot appears fairly robust. Samuels [17] adopted a similar view to that of Lester & Hasan, but also included bitter, ovoid-fruited forms, and a wider distribution range, covering Pakistan, northern and central India and Sri Lanka (Table 1). Recently, purely feral forms have been referred to as S. cumingii/S. melongena subsp. cumingii (Dunal) J. Samuels [6, 18]. 131 132 Other authors have suggested a broader species concept of S. insanum, and have applied the name to the low-growing forms of Lester and Hasan, as well as erect, non-prickly, larger-fruited forms, found across India, Sri Lanka and Bangladesh [19, 20; Table 1]. Alternative circumscriptions [21, 22] have included the straggly forms (see Figure 1), combined with erect forms (sometimes known as S. melongena group F [7]) with moderate armature and smaller, spherical fruits, that are found across South and South-east Asia, and south-eastern China (see Table 1). Madagascar and Mauritius are sometimes included in the distribution range of S. insanum [22]. 4. Hybridisation Wide morphological variability in S. insanum has been described [22, 23, 24] and may reflect the polymorphic nature, typical of many solanums, and its expression in feral brinjal forms. Considerable evidence suggests that S. insanum is of hybrid origin [e.g. 19, 20, 25] and this provides an additional explanation of such variation. Experimentally, S. melongena has been shown to hybridise with around ten of its “spiny Solanum” relatives, including S. insanum, found in India and elsewhere [17, 24, 26]. In addition, some authors assert that brinjal and its wild relatives may freely interchange genes in nature by natural hybridisation [11, 22, 27, 28]. This has been demonstrated by the kind of genetic pattern observed by Mutegi et al. [29]. Using SSR marker analysis, they found that there was no clear genetic separation between sympatric populations of S. melongena and S. insanum in southern India. They suggested that gene flow between the populations contributed towards the shared genetic structure and that this was evidence for conspecificity of the two taxa. Morphologically [22], the two appear to lie on the same spectrum of continuous variation, and reproductively [7, 24, 26] they are interfertile-these features also support conspecificity. Several authors have opted to maintain S. insanum as a synonym of S. melongena [e.g. 18]. Outcrossing in brinjal, facilitated by insects, may be as high as 52.5% [29]. Many of those visiting brinjal are not species-specific, and pollen transfer between brinjal and other Solanum species with comparable phenologies can freely occur; if there is cross-compatibility, viable hybrids will be formed. Thus, the hybrid origin of wild populations identified as S. insanum must be considered, and crosses with species that are extraneous to the primary genepool would account for some of the wider variation that is observed. 5. Introgression According to Karihaloo and colleagues [19, 20] S. insanum in the broad sense is a complex assemblage of “progenitor and derived forms.” The “S. insanum sensu lato” of Karihaloo and Rai [20] can thus exchange pollen reciprocally with taxa within the primary genepool, as well as with hybrids arising amongst these, or even with those involving other wild relatives. Continued backcrossing between hybrid offspring and parents will lead to introgression. It is suggested here that in localities suffering habitat disturbance (such as roadsides and village borders) this will be encouraged because of the availability of many diverse microniches and the adventive nature of spiny solanums. As a result, hybrid swarm populations, based on reticulate webs of hybridisation and introgression amongst brinjal and sympatric wild relatives, are likely to develop. The taxonomic status and appropriate nomenclature of such populations present a challenge.