Increased resolution in the face of conflict: phylogenomics of the Neotropical bellflowers (Campanulaceae: Lobelioideae), a rapid plant radiation

Background and Aims- The centropogonid clade (Lobelioideae: Campanulaceae) is an Andean-centered rapid radiation characterized by repeated convergent evolution of morphological traits, including fruit type and pollination syndromes. While previous studies have resolved relationships of lineages with fleshy fruits into subclades, relationships among capsular species remain unresolved. This lack of resolution has impeded reclassification of non-monophyletic genera, whose current taxonomy relies heavily on traits that have undergone convergent evolution. Methods- Targeted sequence capture using a probeset recently developed for the centropogonid clade was used to obtain phylogenomic data from DNA extracted from both silica-dried and herbarium leaf tissue. These data were used to infer relationships among species using concatenated and partitioned species tree methods, and to quantify gene tree discordance. Key Results- While silica-dried leaf tissue resulted in more and longer sequence data, the inclusion of herbarium samples improved phylogenetic reconstruction. Relationships among baccate lineages are similar previous studies, though differ within and among capsular lineages. We improve phylogenetic resolution of Siphocampylus, which forms ten groups of closely related species which we informally name. Two subclades of Siphocampylus and two individual species are rogue taxa whose placement differs widely across analyses. Gene tree discordance (including cytonuclear discordance) is rampant. Conclusions- The first phylogenomic study of the centropogonid clade considerably improves our understanding of relationships in this rapid radiation. Differences across analyses and the possibility of additional lineage discoveries still hamper a solid and stable reclassification. Rapid morphological innovation corresponds with a high degree of phylogenomic complexity, including cytonuclear discordance, nuclear gene tree conflict, and well-supported differences between analyses based on different nuclear loci. Taken together, these results point to a potential role of hemiplasy underlying repeated convergent evolution. This hallmark of rapid radiations is likely present in many other species-rich Andean plant radiations.

Sending private messages: Floral ultraviolet signals are correlated with pollination syndromes in Erica

The presence of ultraviolet (UV, wavelengths between 300-400 nm) reflectance in insect-pollinated flowers has been linked to pollination efficiency and pollination shifts, but little is known about its prevalence and function in other pollination systems and African species. We chose the genus Erica for studying the prevalence of UV because of its extreme radiation (c. 680 species) in the Cape, South Africa, with a diversity of pollination syndromes. This study quantified the prevalence and brightness of UV reflectance for five Erica pollination syndromes and tested pollinator preferences for UV reflectance in the two groups with the highest prevalence: sunbirds and long-proboscid flies. Our results show that UV colouration is absent or rare in Erica species pollinated by unclassified insects, rodents or wind. About 17 % of bird-pollinated species reflected UV but choice experiments revealed that free-ranging sunbirds showed no preference for UV signals. All sampled long-proboscid fly-pollinated species reflected UV and its experimental removal decreased seed set drastically, suggesting that long-proboscid flies in the Cape strongly prefer or depend on UV and thereby contributed to selecting for the evolution of this signal.

Acoustic traits of bat-pollinated flowers compared to flowers of other pollination syndromes and their echo-based classification using convolutional neural networks

Bat-pollinated flowers have to attract their pollinators in absence of light and therefore some species developed specialized echoic floral parts. These parts are usually concave shaped and act like acoustic retroreflectors making the flowers acoustically conspicuous to the bats. Acoustic plant specializations only have been described for two bat-pollinated species in the Neotropics and one other bat-dependent plant in South East Asia. However, it remains unclear whether other bat-pollinated plant species also show acoustic adaptations. Moreover, acoustic traits have never been compared between bat-pollinated flowers and flowers belonging to other pollination syndromes. To investigate acoustic traits of bat-pollinated flowers we recorded a dataset of 32320 flower echoes, collected from 168 individual flowers belonging to 12 different species. 6 of these species were pollinated by bats and 6 species were pollinated by insects or hummingbirds. We analyzed the spectral target strength of the flowers and trained a convolutional neural network (CNN) on the spectrograms of the flower echoes. We found that bat-pollinated flowers have a significantly higher echo target strength, independent of their size, and differ in their morphology, specifically in the lower variance of their morphological features. We found that a good classification accuracy by our CNN (up to 84%) can be achieved with only one echo/spectrogram to classify the 12 different plant species, both bat-pollinated and otherwise, with bat-pollinated flowers being easier to classify. The higher classification performance of bat-pollinated flowers can be explained by the lower variance of their morphology.

Floral evolution and pollinator diversification in Hedychium J.Koenig (Zingiberaceae): one of Mr. Darwin’s tropical fantasies

ABSTRACTPREMISEHedychium J.Koenig (ginger lilies: Zingiberaceae) is endemic to the Indo-Malayan Realm (IMR) and is known for its fragrant flowers. Two different pollination syndromes characterize the genus: diurnal or bird pollination and nocturnal or moth pollination systems. To date, no attempt has been undertaken to understand the evolution of floral traits in this genus.METHODSWe estimated ancestral character-states, phylogenetic signals, and character correlations for thirteen discrete and eight continuous floral traits representing 75% species diversity of Hedychium. Diversification rate estimation analyses were also employed to understand trait-dependent diversification in the genus.RESULTSInflorescence structure, cincinnus capacity, and curvature of floral tubes revealed strong phylogenetic dependence, whereas number of open flowers per inflorescence per day, color of the labellum, and exertion of the stigma characterized higher ecological effects. Diversification rate estimations suggested that the labellum width, floral tube length, and labellum color played a major role in the evolutionary diversification of Hedychium.CONCLUSIONSWe identified bract type and cincinnus capacity as synapomorphies for Hedychium, while the island-specific clade III was characterized by slender cylindrical inflorescence, coiling of floral tubes, and longer bract to calyx ratio. The circum-Himalayan clade IV is the most speciose, derived, and with most variable floral traits. Although floral color and size lacked any association with pollinator-specific traits (moth and bird pollination), pale colored flowers were most common in the early diverging clades (clade I, II-el., and II-de.), indicating their ancestral nature, when compared to brightly colored flowers.

By wind or wing: pollination syndromes and alternate bearing in horticultural systems

Cyclical fluctuations in reproductive output are widespread among perennial plants, from multi-year masting cycles in forest trees to alternate bearing in horticultural crops. In natural systems, ecological drivers such as climate and pollen limitation can result in synchrony among plants. Agricultural practices are generally assumed to outweigh ecological drivers that might synchronize alternate-bearing individuals, but this assumption has not been rigorously assessed and little is known about the role of pollen limitation as a driver of synchrony in alternate-bearing crops. We tested whether alternate-bearing perennial crops show signs of alternate bearing at a national scale and whether the magnitude of national-scale alternate bearing differs across pollination syndromes. We analysed the Food and Agriculture Organization of the United Nations time series (1961–2018) of national crop yields across the top-producing countries of 27 alternate-bearing taxa, 6 wind-pollinated and 21 insect-pollinated. Alternate bearing was common in these national data and more pronounced in wind-pollinated taxa, which exhibited a more negative lag-1 autocorrelation and a higher coefficient of variation (CV). We highlight the mutual benefits of integrating ecological theory and agricultural data for (i) advancing our understanding of perennial plant reproduction across time, space and taxa, and (ii) promoting stable farmer livelihoods and global food supply. This article is part of the theme issue ‘The ecology and evolution of synchronized seed production in plants’.

Flora of Ferruginous Outcrops Under Climate Change: A Study in the Cangas of Carajás (Eastern Amazon)

Climate change has impacted biodiversity, affecting species and altering their geographical distribution. Besides understanding the impact in the species, it has been advocated that answering if different traits will be differently impacted could allow refined predictions of how climate change will jeopardize biodiversity. Our aim was to evaluate if climate change will potentially impact plant species differently, considering their traits. We evaluated 608 plant species that occur in the naturally open areas of ferruginous outcrops (namely, cangas) in the National Forest of Carajás (Eastern Amazon). Firstly, we estimated the effects of climate change on each species using species distribution modeling, and analyzed this impact in the set containing all species. Secondly, we classified plant species considering the following traits: (i) pollination syndromes (melittophily, phalaenophily, psychophily, cantharophily, entomophily, ornithophily, chiropterophily, anemophily); (ii) habit (tree, shrub, herb, liana, parasite); and (iii) the main habitat of occurrence (open areas and forests). Thirdly, we investigated if the effects of climate change could be significantly more intense considering all the different traits quoted. Our results showed that most plant species will potentially face reduction of suitable habitats under future climate and the scenarios showed that 42% of them may not find suitable areas in the cangas of Carajás. We found no significant difference within each analyzed trait, considering the potential impact of climate change. The most climatically suitable areas (i.e., areas with high probability of species occurrence in the future) are those in the southwest of the study area. These areas can be considered as priority areas for species protection against climate change.

Variation in Manduca sexta Pollination-Related Floral Traits and Reproduction in a Wild Tobacco Plant

Most flowering plants depend on animal pollination for successful sexual reproduction. Floral signals such as color, shape, and odor are crucial in establishing this (often mutualistic) interaction. Plant and pollinator phenotypes can vary temporally but also spatially, thus creating mosaic-like patterns of local adaptations. Here, we investigated natural variation in floral morphology, flower volatile emission, and phenology in four accessions of a self-compatible wild tobacco, Nicotiana attenuata, to assess how these traits match the sensory perception of a known pollinator, the hawkmoth Manduca sexta. These accessions differ in floral traits and also in their habitat altitudes. Based on habitat temperatures, the accession occurring at the highest altitude (California) is less likely to be visited by M. sexta, while the others (Arizona, Utah 1, and Utah 2) are known to receive M. sexta pollinations. The accessions varied significantly in flower morphologies, volatile emissions, flower opening, and phenology, traits likely important for M. sexta perception and floral handling. In wind tunnel assays, we assessed the seed set of emasculated flowers after M. sexta visitation and of natural selfed and hand-pollinated selfed flowers. After moth visitations, plants of two accessions (Arizona and Utah 2) produced more capsules than the other two, consistent with predictions that accessions co-occurring with M. sexta would benefit more from the pollination services of this moth. We quantified flower and capsule production in four accessions in a glasshouse assay without pollinators to assess the potential for self-pollination. The two Utah accessions set significantly more seeds after pollen supplementation compared with those of autonomous selfing flowers, suggesting a greater opportunistic benefit from efficient pollinators than the other two. Moreover, emasculated flowers of the accession with the most exposed stigma (Utah 2) produced the greatest seed set after M. sexta visitation. This study reveals intraspecific variation in pollination syndromes that illuminate the potential of a plant species to adapt to local pollinator communities, changing environments, and altered pollination networks.