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Research Article
Impatiens smetsiana, another example of convergent evolution of flower morphology in Impatiens
expand article infoSteven B. Janssens‡§, Hermann Taedoumg|, Steven Dessein‡
‡ Meise Botanic Garden, Meise, Belgium
§ KU Leuven, Leuven, Belgium
| University of Yaoundé, Yaoundé, Cameroon
¶ Alliance Bioversity International–CIAT, Yaoundé, Cameroon

Corresponding author: Steven B. Janssens ( steven.janssens@plantentuinmeise.be )

Academic editor: João Farminhão
© 2022 Steven B. Janssens, Hermann Taedoumg, Steven Dessein.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Janssens SB, Taedoumg H, Dessein S (2022) Impatiens smetsiana, another example of convergent evolution of flower morphology in Impatiens. Plant Ecology and Evolution 155(2): 248-260. https://doi.org/10.5091/plecevo.89701
Open Access

Abstract

Background and aims – The genus Impatiens is known for its enormous convergent phenotypic adaptation, with similar floral traits having independently evolved in distantly related lineages. The large functional convergence of Impatiens flowers causes a high degree of homoplasy for several phenotypic characters resulting in increased difficulties to distinguish between species with a similar morphology that are only distantly related, however. As a result, some species remain under the radar, as they are confused with other well-known species. This was the case for a new Impatiens species from the Tchabal Mbabo Mountains in Cameroon – Impatiens smetsiana – that was initially mistaken for the morphologically similar species I. erecticornis, an endemic from Central East Africa.

Material and methods – A combined molecular-morphological approach was applied in which phylogenetics (ITS, ImpDEF1, and ImpDEF2), biogeography, and age estimation analyses were combined with morphological data on floral and vegetative structures.

Key results – In this study, we demonstrate the close affinity of the newly collected material with a group of Equatorial West African species, including I. filicornu, I. nzabiana, I. oumina, and I. kamerunensis. The present finding represents a clear case of convergent evolution in which two distantly related taxa independently converged on practically the same flower morphology.

Conclusion – Within Impatiens, several examples of floral homoplasy have been observed yet not in such a clear way. The convergent evolution of the flowers of I. smetsiana and I. erecticornis is undoubtedly closely correlated with an adaptation to a similar pollination syndrome.

Keywords

Adamawa, biogeography, Cameroon, convergent evolution, diversification, Impatiens, speciation

Introduction

Although Hooker made an initial revision of the Indian representatives of the genus Impatiens L. in 1859 (Hooker and Thomson 1859), it took him more than 40 years to recommence his study on Indian balsams. In fact, he spent the last 10 years of his life trying to unravel the complex diversity of the genus and came to the conclusion that Impatiens are ‘a terror to botanists, deceitful above all plants and desperately wicked’ (Hooker 1875, 1905; Huxley 1918; Grey-Wilson 1980). Already during his first survey, Hooker points to the huge floral variety that is present within Impatiens stating that ‘it would be difficult to indicate another genus in the vegetable kingdom, presenting amongst its species so many and such different modifications of structure, and of which the species are so excessively prone to vary’ (Hooker and Thomson 1859). As a result of this floral variation, it has always been very difficult to divide the genus into natural groupings using solely morphological data (Hooker and Thomson 1859; Warburg and Reiche 1895; Hooker 1905). The genus Impatiens is known for its enormous convergent phenotypic adaptation, with similar floral traits having independently evolved in distantly related lineages (Yuan et al. 2004; Janssens et al. 2006, 2009b; Yu et al. 2015; Vandelook et al. 2019; Abrahamczyk et al. 2021; Ruchisansakun et al. 2021). The large functional convergence of Impatiens flowers causes a high degree of homoplasy for several phenotypic characters. In general, it is assumed that the majority of convergent traits are the result of an adaptation for particular ecological conditions. Moreover, morphological adaptation to pollinators is considered to be a widespread phenomenon in floral evolution as there is often a strong selection towards certain floral traits due to behaviour and morphology of the pollinator (Okuyama et al. 2008). Phylogenetic analyses have demonstrated that most of the phenotypic homoplasy in Impatiens is the result of convergent evolution (Yuan et al. 2004; Janssens et al. 2006, 2007, 2008).

Grey-Wilson (1980) highlights the occurrence of floral morphological similarities between species endemic to India, Africa, Madagascar, and Southeast Asia and assumes a clear affinity between those species. However, recent molecular analyses showed that the intrageneric relationships within Impatiens are strongly geographically structured, with each main clade restricted to a specific geographic area and hardly any amalgamation of geographically different taxa in a single clade (Yuan et al. 2004; Janssens et al. 2006, 2007, 2009a; Yu et al. 2015; Ruchisansakun et al. 2016). In addition, these studies revealed the enormous homoplastic nature of floral characters in Impatiens. Despite the clear evidence of convergent evolution in several different Impatiens lineages (e.g. red flowered species with bucciniform spurred sepals: I. niamniamensis Gilg (Central Africa), I. parasitica Bedd. (South India), and I. humblotiana Baill (Madagascar); pink flowered species with a filiform spur: I. walleriana Hook.f. (East Africa), I. lyallii Baker (Madagascar), I. latifolia L. (South India), and I. hawkeri W.Bull (Papua New Guinea)), this convergence occurs especially in certain floral traits (e.g. the spurred sepal, the lateral united petals, and the dorsal petal). Despite the overall similarity in flower morphology between two convergent Impatiens species, slight morphological differences between the species remain present. For the non-trained eye, however, it is often difficult to spot these small dissimilarities between different species, resulting in an underestimation of the real number of species for a certain lineage. For example, within Impatiens, several recently described species were originally identified as a morphologically similar but less closely related species (e.g. Janssens et al. 2009b, 2010, 2011). The present paper investigates the convergent relationship of a new Impatiens species with its morphological doppelgänger for which it was originally mistaken for. The new species is described and illustrated, and its evolutionary history is studied using biogeographic analyses and age estimation analyses.

Material and methods

Morphological description and data analysis

Two accessions of the new species were collected by the second and last author in May 2009. The material was collected in northern Cameroon (Adamawa region). Descriptive terminology follows Grey-Wilson (1980) except for simple symmetrical plane shapes (SACDBT 1962).

In order to study the convergent evolution of I. smetsiana and I. erecticornis R.Wilczek & G.M.Schulze, we analysed the overall morphology of those two species with the closest allies of I. smetsiana using a Multiple Factor Analysis for mixed data (continuous and discrete) as implemented in the FactoMineR R package (Lê et al. 2008). The scores obtained for each individual in the first two dimensions were used to interpret the degree of phenotypical convergence between the new species and its morphological doppelgänger, I. erecticornis. Morphological traits used in the analysis are provided in Table 1.

Table 1.
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Comparison of taxonomic useful characters of the species closely related to I. smetsiana and the morphologically similar I. erecticornis. Size indicates both measurements for length and width, respectively.

I. erecticornis I. filicornu I. smetsiana I. kamerunensis subsp. kamerunensis I. kamerunensis subsp. obanensis I. nzabiana
Height (cm) 40–150 35 40–60 40 50–60 (100) 40
Leaf arrangement spirally spirally spirally opposite-subopposite spirally spirally
Petiole length(cm) 1.2–7.5 2.5–6 2–6.3 0.5–4 0.5–4 1.2–2.5
Leaf size (cm) 5.4–14.3 × 2.4–7.0 3.2–8.5 × 1–5 7.5–11 × 3.7–4.5 2.8–10 × 1.6–3.8 4.3–14 × 2.2–7.0 3–5 × 0.9–1.3
Leaf shape ovate ovate-narrowly ovate (elliptic) elliptic ovate, oblong-narrowly ovate ovate, oblong-narrowly ovate narrowly ovate-rhombic to narrowly elliptic
Leaf apex acuminate acute to shortly acuminate acuminate acute to acuminate acute to acuminate acuminate
Leaf base cuneate- attenuate attenuate-rounded attenuate rounded-shortly attenuate rounded-shortly attenuate cuneate
Lateral veins 7–10 pairs 4–5(–6) pairs 5–7 pairs 4–9 pairs 4–9 pairs 6–8 pairs
Leaf margin crenate shallowly crenate crenate shallowly crenate to crenate-serrate shallowly crenate to crenate-serrate finely crenate-serrate
Fimbriae present present absent often present often present present
Inflorescence 3–6 flowered subumbellate raceme 4–9 flowered subumbellate raceme 6–many flowered subumbellate raceme lax 6–many flowered axillary or pseudo-terminal raceme lax 6–many flowered axillary or pseudo-terminal raceme lax axillary racemes
Flower colour pink pink-purplish pink pink-purplish pink-purplish pink
Peduncle length (cm) 3–9.5 8–14 5.5–14 5.5–16 5.8–26 11–12
Bract size (mm) 5–8 × 4–6 3–6 × 3–4 5–6 × 4–5 2–4.5 2–4.5 1
Bract shape ovate ovate ovate ovate lanceolate to linear lanceolate ovate lanceolate to linear lanceolate linear lanceolate
Lateral sepal length (mm) 6–7 3–4 3.8–4.5 2.5–4 2.5–4 1.2
Lateral sepal shape ovate ovate ovate ovate lanceolate to linear lanceolate ovate lanceolate to linear lanceolate narrowly and obliquely navicular
Lower sepal length (mm) 9–11 5 8–9 3–6 4–9 7–8
Spur length (mm) 23–28 10–35 23–35 13–30 35–55 22.5–25
Spur shape curved filiform curved filiform curved filiform curved filiform curved filiform curved and flattened filiform
Dorsal petal size (mm) 6–8 × 4–6 4.4 × 4.0 10.5 × 9.5 3–13 × 3–10 3–13 × 3–10 5–6 × 7–8
Dorsal petal shape cucullate oblong oblong-shallowly cucullate oblong-suborbicular oblong-suborbicular suborbicular
Lateral united petals length (mm) 24–35 10–16 19–21 12–15 16–20 16.5–18.0
Upper lateral petal size (mm) 13–19 × 7–11 8 × 2–3 12–13 × 8–9 7–13 × 3–10 7–13 × 3–10 12.0–13.5 × 5
Upper lateral petal shape oval-kidney shaped narrowly oblong-elliptic oval-kidney shaped transversely and broadly oblong to ± kidney shaped transversely and broadly oblong to ± kidney shaped narrowly oblong
Lower lateral petal size (mm) 15–27 × 8–13 8–10 × 6–8 15.5–16.5 ×12.5–13 3–10 × 5.5–13 3–10 × 5.5–13 14.5–15.0 × 8.0–8.5
Lower lateral petal shape asymmetrically obovate suborbicular-oblong asymmetrically obovate suborbicular to obliquely oblong suborbicular to obliquely oblong suborbicular
Size ligulate appendage of lower lateral petal (mm) not applicable 3–5 × 1–2 4–4.5 × 2.5–4.1 3–7 × 1–2.5 3–7 × 1–2.5 7.0–7.5 × 2.5–3.0
Fruit length (mm) 9–15 13–5 mm unknown 9–17 9–17 6.5

Phylogenetic analyses

In order to determine the phylogenetic position of I. smetsiana among the African lineages, we added sequences of the new species to a combined nuclear ImpDEF1/ImpDEF2 and nuclear ribosomal ITS data matrix. Based on earlier phylogenetic studies (Volkmar et al. 2014), I. rubrostriata Hook.f. and I. conchibracteata Y.L.Chen & Y.Q.Lu serve as outgroup species. Total genomic DNA was isolated from silica-dried leaf material using a modified CTAB protocol (Doyle and Doyle 1987), which is optimized for Impatiens by Janssens et al. (2006, 2009b). Primers and temperature profiles used for the amplification of ImpDEF1/ImpDEF2, and ITS follow Janssens et al. (2007, 2008) and White et al. (1990), respectively. Amplification reactions were carried out on a GeneAmp PCR system 9700 (Applied Biosystems). Purified amplification products were sent to Macrogen, Inc. (Seoul, South Korea) for sequencing. Sequences obtained in this study were submitted to GenBank (Supplementary file 1).

Contiguous sequences were assembled using Geneious v.7.0.6 (Biomatters, New Zealand). Automatic alignments were carried out with MAFFT (Katoh et al. 2002) under an E-INS-i algorithm, a 100PAM/k=2 scoring matrix, a gap open penalty of 1.3 and an offset value of 0.123. Subsequent manual fine-tuning of the aligned dataset was done in Geneious v.7.0.6. Congruency between the different datasets was inferred using different methods. First, a series of incongruence length difference tests (ILD; Farris et al. 1995) were carried out with PAUP* v.4.0b10 (Swofford 2003) using the following parameters: simple taxon addition, TBR branch swapping, and heuristic searches of 1000 repartitions of the data. Despite the well-known sensitivity of the ILD test (Barker and Lutzoni 2002), the results of this test were compared in light of the resolution and support values of the obtained nuclear and nuclear ribosomal topologies. As a result, possible conflict between data matrices was visually inspected, searching for conflicting relationships within each topology that are strongly supported (hard vs soft incongruence; Johnson and Soltis 1998).

The best-fit nucleotide substitution model for each plastid and nuclear dataset was selected using jModelTest v.2.1.4. (Posada 2008) out of 88 possible models under the Akaike information criterion (AIC). The GTR+I+G model was found as best fit for ImpDEF1, whereas the GTR+G model was calculated as best substitution model for ImpDEF2 and ITS. As a result, we used a mixed-model approach to apply different evolutionary models on each DNA region of the combined dataset (Ronquist and Huelsenbeck 2003). Bayesian inference analyses were conducted with MrBayes v.3.1 (Huelsenbeck and Ronquist 2001) on four individual data partitions and a combined data matrix. Each analysis was run two times for 20 million generations. Trees were sampled every 5,000th generation. Chain convergence and ESS parameters were inspected with TRACER v.1.4 (Rambaut and Drummond 2007). Only nodes with Bayesian posterior probabilities (BPP) above 0.95 are considered as well supported (Suzuki et al. 2002). Maximum Likelihood analyses were conducted using the RAxML search algorithm (Stamatakis et al. 2005) as implemented in RAxML v.7.2.8 (Stamatakis et al. 2008) under the GTRGAMMA approximation of rate heterogeneity for each gene (Stamatakis 2006). Five hundred bootstrap trees were inferred using the RAxML Rapid bootstrap algorithm (ML-BS) to provide support values for the best-scoring ML tree.

Divergence time estimation

The molecular clock hypothesis was tested using a chi2 likelihood ratio test (Felsenstein 1988) and demonstrated that the substitution rates in the combined dataset are not clock-like (p < 0.001 for all markers). BEAUti v.1.8.0 (Drummond and Rambaut 2007) was used to prepare the xml file prior to the dating analysis in BEAST v.1.8.0 (Drummond and Rambaut 2007). The latter software program applies the Bayesian methodology to compute divergence times. However, in order to surpass the zero likelihood issue in BEAST, we used a starting tree that was obtained by carrying out a ML analysis in RAxML v.7.2.8 (Stamatakis et al. 2008) under GTRGAMMA model with the rooted likelihood tree as input tree for a penalized likelihood (PL) analysis in the software program r8s (Sanderson 2003). Due to differing substitution models among the different gene markers used, a partitioned Bayesian MCMC analysis was performed under the Yule speciation model and a relaxed lognormal clock. Partitions were unlinked for the model of evolution. The analysis ran for 30 million generations and was sampled each 5,000th generation. Convergence of the chains and ESS parameter evaluation (ESS > 200) was performed with TRACER v.1.6 (Rambaut and Drummond 2007). A maximum clade credibility tree using a posterior probability limit of 0.5 was calculated using TreeAnnotator v.1.8.0. (Drummond and Rambaut 2007). The previously computed age estimate for the most recent common ancestor of the Afro-Madagascan and Equatorial West African clades of Janssens et al. (2009a) was used to calibrate the ingroup of the current study. This calibration point was given a normal distribution with a mean value of 7.87 Ma and a standard deviation of 0.5.

Results

Morphological data analysis

The first two components of the multivariate analysis explained 69% of the total variation in continuous traits. Dimension 1 correlated with upper lateral petal shape, leaf apex, flower colour, bract shape, and lateral sepal size. Dimension 2 with dorsal petal shape, lower lateral petal shape, inflorescence, and to a lesser extent leaf margin and petiole length. The multiple factor analysis for mixed data demonstrates that Impatiens smetsiana (Fig. 1A–B) and its morphological doppelgänger I. erecticornis (Fig. 1D) cluster well together (Fig. 2). This clustering is mainly the result of overall similarities in floral morphology between both species and to a lesser extent because of similarities in vegetative morphology. In addition to the morphological resemblance of I. smetsiana and I. erecticornis, also I. kamerunensis subsp. obanensis and I. kamerunensis subsp. kamerunensis aggregate well in the cluster analysis (Fig. 2).

Figure 1. 

A. Frontal view of I. smetsiana flower. B. Lateral view of I. smetsiana flower. C. Frontal view of I. kamerunensis subsp. kamerunensis flower. D. Frontal view of I. erecticornis flower. A–B: Dessein & Taedoumg 2971 (BR [BR0000034048368]); C: Dessein et al. 2673 (BR [BR0000005605668]); D: Fischer s.n. (BONN). Photos by: A–C: Steven Dessein, D: Eberhard Fischer.

Figure 2. 

Multivariate plot based on variation in morphological characters (continuous and discrete) of Table 1 obtained by a Multiple Factor Analysis for mixed data.

Phylogenetic analyses

No significant incongruence between ITS and ImpDEF1/ImpDEF2 (p > 0.05) was found using the partition homogeneity test. Visual examination of the two different partitions of the combined dataset corroborates this congruency analysis. ML and BI analysis of the combined dataset generated topologies with moderate to high support values (Fig. 3).

Impatiens smetsiana is part of a small clade consisting only of Equatorial West African species (Fig. 3). Phylogenetic analyses indicate that I. smetsiana is sister to a clade containing I. oumina, I. nzabiana, I. kamerunensis subsp. kamerunensis, and I. kamerunensis subsp. obanensis (ML: 65, BI: 0.91). Impatiens filicornu Hook.f. is sister to this entire clade (ML: 94, BI: 1.00). The clade formed by the novelty, and the above-mentioned Impatiens species [((((I. nzabiana, I. oumina) (I. kamerunensis subsp. kamerunensis, I. kamerunensis subsp. obanensis)) I. smetsiana) I. filicornu)] is sister to the extant species of the Equatorial West African Impatiens clade, except I. sakeriana, which is the most early divergent species of this Equatorial West African lineage (Janssens et al. 2009a).

Divergence time estimation

Within twenty million generations, stationarity among the different chains as well as ESS values over 200 were obtained. The BEAST maximum clade credibility tree analysis is depicted in Fig. 3. Divergence time for Equatorial West African lineage corroborates the study of Janssens et al. (2009a) and is estimated at 3.67 Ma (4.99–2.74 Ma (95% highest priority density (HPD))) (Fig. 3). Additionally, time divergence estimates of the Afro-Madagascan clade to which I. erecticornis belongs are in accordance with earlier dating analyses of Janssens et al. (2009a), having a mean age of 4.43 Ma (5.39–3.46 Ma (95% HPD)). The split between I. erecticornis and its sister species (I. bequaertii) is situated in the Pleistocene (2.32 Ma (3.25–1.24 Ma (95% HPD)), suggesting a Pleistocene origin. The stem node age of I. smetsiana is situated in the a Pliocene at 2.61 Ma (3.64–1.73 Ma (95% HPD)).

Figure 3. 

Maximum clade credibility inferred from combined ITS, ImpDEF1, and ImpDEF2 as obtained from the BEAST software program. Numbers on branches represent Bayesian Posterior Probabilities and Maximum Likelihood Bootstrap Support, respectively. Blue bars indicate age intervals (95% HPD credibility).

Discussion

Diagnostic characters and relationships

Examination of the general morphological characters of I. smetsiana shows that the novelty is morphologically very similar to I. erecticornis in general appearance: spirally arranged leaves with acuminate leaf apex and attenuate leaf base, subumbellate racemes, ovate bracts and lateral sepals, a curved filiform spur, oval-kidney shaped upper lateral petals and asymmetrically obovate lower lateral petals and equally sized lateral petals. Impatiens smetsiana differs from I. erecticornis in leaf shape (elliptic vs ovate), the absence of fimbriae at the base of the leaf margins, the number of secondary veins (5–7 vs 7–10), the number of flowers per inflorescence (> 6 vs 3–6), and the dorsal petal lacking a distinct crest. Despite the morphological resemblance, molecular analyses indicate that I. erecticornis is part of a distinct clade of Equatorial East African species that are only distantly related to the Equatorial West African lineage to which I. smetsiana belongs. The most recent common ancestor of both species is located in Southwest China around 7.87 Ma (Janssens et al. 2009a). To date, I. erecticornis is only found in eastern DR Congo and in western Rwanda (Albertine Rift) (Fischer 1997).

Furthermore, molecular phylogenetic analyses demonstrated the close affiliation of I. smetsiana with the morphologically more distinct species I. filicornu, I. kamerunensis subsp. kamerunensis, I. kamerunensis subsp. obanensis, I. nzabiana, and I. oumina. Although there are still some common morphological characteristics between the novelty and the first four species mentioned here, there is only limited morphological resemblance with I. oumina and I. nzabiana except for a simple or sparsely branched stem and spirally arranged leaves (Janssens et al. 2011). When comparing I. smetsiana with the two I. kamerunensis subspecies, it is clear that I. kamerunensis subsp. obanensis is morphologically more similar to the new species than I. kamerunensis subsp. kamerunensis. Only the morphological character spur length of the new species falls in between that of the two subspecies of I. kamerunensis. In comparison to I. kamerunensis subsp. kamerunensis, the new species is significantly larger in overall size (on average between 50 and 60 cm in height), has spirally arranged leaves instead of an opposite-subopposite leaf arrangement, a larger lower sepal (up to 9 mm long) and larger lateral petals (19–21 mm), four characters it shares with I. kamerunensis subsp. obanensis. In addition, I. smetsiana differs from I. kamerunensis s.l. in having a subumbellate raceme instead of a lax axillary or pseudo-terminal raceme, and a distinct shape of the united lateral petals. Although molecular analyses strongly support a sister group relationship of I. smetsiana with I. nzabiana, I. oumina, and I. kamerunensis s.l., the novelty has also several morphological characters in common with the more early branched off I. filicornu. Impatiens filicornu is similar to I. smetsiana by the presence of a simple or sparsely branched stem with spirally arranged leaves, subumbellate racemes, ovate bracts and lateral sepals, and pink flowers with a whitish filiform spur. However, it can be easily distinguished from the new species by the presence of fimbriae at the leaf base, the smaller size of both plants and flowers, and the narrowly oblong-elliptic upper lateral petals and suborbicular-oblong lower lateral petals.

Convergent flower morphology in Impatiens: I. smetsiana vs I. erecticornis

Unravelling higher level taxonomic relationships in Impatiens based on morphological data has proven difficult due to the huge floral variation present in the genus (Hooker and Thomson 1859; Hooker 1875, 1905; Warburg and Reiche 1895). Recent molecular phylogenetic analyses identified large incongruence between molecular data and morphological characters in which similar flower types are randomly distributed throughout the phylogeny (Yuan et al. 2004; Janssens et al. 2006; Yu et al. 2015). The study of Janssens et al. (2006) demonstrated that the main Impatiens lineages are biogeographically delimited to one of the major hotspots for the genus. Interestingly, in each of these biogeographically delimited clades in Africa, Madagascar, South India, and Southeast Asia, there is a trend of convergent flower evolution with the independent development of the same major flower types: (1) flat flower type with a shallow lower sepal and long filiform spur, (2) funnel flower type with cucullate dorsal petal, deeply navicular lower sepal and short filiform spur, (3) funnel flower type with cucullate dorsal petal, large saccate lower sepal and bucciniform spur. In general, homoplasy of similar floral characters amongst biogeographically delimited lineages within Impatiens is fairly obvious to recognize, as the development of each of these flower types in each delineated clade is rather distinctive. The present finding is remarkable as it implies a rather pronounced case of convergent evolution in which two distantly related taxa (their MRCA was probably a funnel shaped flower with a saccate spurred sepal; Janssens et al. 2008) independently converged into practically the same flower morphology. It is generally accepted that the convergent evolution of complex phenotypic traits such as the complete turnover of the flower morphology is the result of stochastic processes (Wood et al. 2005). Moreover, the majority of cases in which morphological homoplasy is clearly present appears to be the result of natural selection. As for I. smetsiana and I. erecticornis, the convergent evolution of their flowers is undoubtedly closely correlated with an adaptation to a similar pollination syndrome. The typical floral morphology of the two convergent Impatiens species investigated is exclusively psychophilous (butterfly-pollinated). The shape of the flower causes the pollinator to position itself on the often large lower lateral petals, directly given access to the long nectar spur through a narrow opening between the two pairs of lateral petals underneath the stamens. With its long proboscis, the butterfly can easily access the nectar, which is situated near the tip of the spur. Morphological homoplasy is often suggested to be the outcome of unique genetic changes. In such an extreme case of convergent evolution in which complex floral morphological traits evolved several times, one could assume that only a few major quantitative trait loci (QTLs) are involved. This would cause the number of pathways from phenotype ‘A’ to phenotype ‘B’ to be significantly limited and thus increases the possibility of complex morphological homoplasy to occur under a common genetic basis. However, because the dynamics on how genes regulate the eventual flower morphology in Impatiens is still unclear, it is difficult to say whether convergent evolution of complex morphological traits, as is the case for I. smetsiana and I. erecticornis, have a common genetic background.

Biogeographical understanding of the origin of I. smetsiana

Molecular data demonstrates that I. smetsiana is only very distantly related to its morphological doppelgänger I. erecticornis endemic to the Albertine Rift, but is in fact closely related to the Impatiens species of the Equatorial West African clade containing I. kamerunensis subsp. kamerunensis, I. kamerunensis subsp. obanensis, I. nzabiana, and I. oumina. Because I. nzabiana and I. oumina are strict endemics of the Massif du Chaillu (South Gabon) and their divergence time is estimated between 0.61 and 0.017 Ma, both species had most likely no influence on the divergence of I. smetsiana which happened approximately two million years earlier. As a result, we further refer to the Equatorial West African species I. kamerunensis subsp. kamerunensis and I. kamerunensis subsp. obanensis when discussing the biogeography and evolution of I. smetsiana. In contrast to I. smetsiana, which is putatively endemic to the Tchabal Mbabo Mountains in Central North Cameroon (Adamawa Region), I. kamerunensis subsp. kamerunensis and I. kamerunensis subsp. obanensis are more widely distributed and occur in Southwest Cameroon (Northwest, Southwest, West, and Littoral Region), southern Nigeria, Ghana, and Togo. Interestingly, the known distribution area of I. smetsiana does not overlap with that of I. kamerunensis subsp. kamerunensis and I. kamerunensis subsp. obanensis. The montane forests of Tchabal Mbabo to which I. smetsiana is endemic, are part of the Afromontane regional centre of endemism. According to Thomas and Thomas (1996), the Tchabal Mbabo forests are of a rare, dry type, which is completely surrounded by deciduous woodland or shrubland. Impatiens smetsiana was found in a small creek on the north escarpment edge of these montane forests, close to the gallery forests that dissect the plateau grasslands, with a population of I. mackeyana subsp. zenkeri thriving downstream of the novelty. Most likely, the steep slopes of the Tchabal Mbabo montane escarpment forest created an orographic effect resulting in a suitable microclimate for Impatiens populations to grow in that area (Chapman 2004).

Taxonomic treatment

Impatiens smetsiana S.B.Janssens, Taedoumg & Dessein, sp. nov.

urn:lsid:ipni.org:names:77300987-1
Figs 1, 4

Type

CAMEROON – Adamawa Region • Chabal Mbabo; 7°13’54”N, 12°5’57”E; 8 May 2009; Dessein S. & Taedoumg H. 2950; holotype: BR [BR0000024941891]; isotype: L [L.4446681], YA, WAG.

Figure 4. 

Impatiens smetsiana. A. Habit. B. Frontal view of flower. C. Lateral view of flower. D. United lateral petals. E. Dorsal petal. F. Lateral sepals. G. Lower sepal and spur. Drawn by Antonio Fernandez from Dessein & Taedoumg 2971 (BR [BR0000034048368]).

Diagnosis

Impatiens smetsiana belongs to the Equatorial West African Impatiens lineage. It differs from I. kamerunensis, I. filicornu, and I. nzabiana in having an elliptic leaf shape, no leaf fimbriae, an oblong-shallowly cucullate dorsal petal shape, and an asymmetric obovate lower lateral petal shape.

Description

Erect perennial herb up to 60 cm tall. Stems simple or branched, glabrous. Leaves spirally arranged; petiole 2–6.3 cm long; leaf blades 7.5–11 × 3.7–5.5 cm, ± elliptic, attenuate at the base, ± acuminate at the apex, glabrous; lateral veins 5–7 at each side of the midrib; leaf margins crenate without short filiform fimbriae at the base. Flowers in 6 to many flowered subumbellate racemes; pedicels 15–21 mm long, slender, glabrous; bracts green with red tips; ovate, 5–6 × 4–5 mm. Lateral sepals 2, green, 3.8–4.5 mm, ovate, glabrous. Lower sepal pink, 8–9 × 7–7.5 mm, narrowly and obliquely navicular, abruptly constricted into a 23–35 mm long curved filiform white spur. Dorsal petal pink, 10.5 × 9.5 mm, shallowly cuculate, with a shallow narrow dorsal crest. Lateral united petals bright pink with a small white spot at the base of the upper lateral petal of each lateral united pair and a deep pink spot at the base of the lower lateral petal of each pair, 19–21 mm long, with the upper petal of each pair equal in appearance compared to the lower one. Upper petal 12–13 × 8–9 mm, oval-kidney shaped; lower petal of each pair 15.5–16.5 × 12.5–13 mm, asymmetrically obovate, distally produced into 4.0–4.5 × 2.5–4.1 mm ligulate appendage. Stamens 5, alternating with the petals, connate to a ring. Ovary 5-locular, glabrous. Fruits fusiform. Seeds unknown.

Distribution

Impatiens smetsiana is endemic to Cameroon. Only known from Tchabal Mbabo (type location; Fig. 5).

Figure 5. 

Distribution of I. smetsiana (black asterisks) in the Tchabal Mbabo region. Eq.G.: Equatorial Guinea; C.A.R.: Central African Republic; Congo Br.: Congo Brazzaville.

Habitat and ecology

Impatiens smetsiana grows between 1900 and 2100 m, in gallery forest. Following species were collected together with the new Impatiens: Campylospermum sp., Carapa sp., Cassipourea sp., Chassalia sp., Clematis sp., Cremaspora triflora, Echinops sp., Gladiolus sp., Hypoxis sp., Moraea schimperi, Multidentia dichrophylla, Pavetta sp., Pentanisia sp., Peperomia sp., Psychotria moseskemei, Psychotria peduncularis var. peduncularis, Psychotria psychotrioides, Psychotria succulenta, Psydrax kraussioides, Rothmannia sp., and Spermacoce verticillata.

Phenology

Impatiens smetsiana flowers in May (based on two records), fruiting occurs immediately after flowering.

Etymology

The species epithet smetsiana refers to the Belgian botanist, Erik F. Smets.

Preliminary IUCN conservation assessment

Vulnerable: VU D2. The species has been collected twice in a non-protected area in the Chabal Mbabo region. Human pressure in the region (mainly cattle breeding) is significant and results in the degradation and destruction of forested areas (Chapman 2004). Because of the restricted and fragmented distribution range of I. smetsiana, we would apply the category vulnerable under criterion D2. Human activities can make the species become critically endangered or even extinct within a rather short timeframe (IUCN 2012, 2019).

Additional material examined

CAMEROON – Adamawa Region • Chabal Mbabo; 7°14’14”N, 12°5’24”E; 9 May 2009; Dessein S. & Taedoumg H. 2971; BR [BR0000034048368].

Acknowledgements

We thank the curators of BR, LBV, WAG, and YA for making their collections available. Antonio Fernandez is acknowledged for the botanical drawing. This study was financed by research grants of the KU Leuven (OT/05/35) and the Fund for Scientific Research-Flanders (FWO Belgium) (G.0104.01). Both the F.R.S.-F.N.R.S. and the F.F.R.S.A. (Fondation pour Favoriser les Recherches Scientifiques en Afrique) supported our research in Cameroon. Bonaventure Sonké, Murielle Simo-Droissart, and Olivier Lachenaud are acknowledged for their support during the field trip of Steven Dessein and Hermann Taedoumg. Wim Baert and Anja Vandeperre are acknowledged for their help in the lab. Yves Bawin is thanked for his help in the statistical testing of the morphological data. Special thanks to Eberhard Fischer for providing us with photographic material of I. erecticornis.

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Supplementary material

Supplementary material 1 

List of taxa, their localities, voucher information, and GenBank accession numbers (ImpDEF1, ImpDEF2, ITS) for the plant material used in this study.

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