Ingestion of the cycad toxins β-methylamino-L-alanine (BMAA) and azoxyglycosides is harmful to diverse organisms. However, some insects are specialized to feed on toxin-rich cycads with apparent immunity. Some cycad-feeding insects possess a common set of gut bacteria, which might play a role in detoxifying cycad toxins. Here, we investigated the composition of gut microbiota from a worldwide sample of cycadivorous insects and characterized the biosynthetic potential of selected bacteria. Cycadivorous insects shared a core gut microbiome consisting of six bacterial taxa, mainly belonging to the Proteobacteria, which we were able to isolate. To further investigate selected taxa from diverging lineages, we performed shotgun metagenomic sequencing of co-cultured bacterial sub-communities. We characterized the biosynthetic potential of four bacteria from Serratia, Pantoea, and two different Stenotrophomonas lineages, and discovered a suite of biosynthetic gene clusters notably rich in siderophores. Siderophore semi-untargeted metabolomics revealed a broad range of chemically related yet diverse iron-chelating metabolites, including desferrioxamine B, suggesting the occurrence of an unprecedented desferrioxamine-like biosynthetic pathway that remains to be identified. These results provide a foundation for future investigations into how cycadivorous insects tolerate diets rich in azoxyglycosides, BMAA, and other cycad toxins, including a possible role for bacterial siderophores.
Cycads are an ancient group of tropical gymnosperms that are toxic to most animals – including humans – though the larvae of many moths and butterflies (order: Lepidoptera) feed on cycads with apparent immunity. These insects belong to distinct lineages with varying degrees of specialisation and diverse feeding ecologies, presenting numerous opportunities for comparative studies of chemically mediated eco‐evolutionary dynamics. This review presents the first evolutionary evaluation of cycad‐feeding among Lepidoptera along with a comprehensive review of their ecology. Our analysis suggests that multiple lineages have independently colonised cycads from angiosperm hosts, yet only a few clades appear to have radiated following their transitions to cycads. Defensive traits are likely important for diversification, as many cycad specialists are warningly coloured and sequester cycad toxins. The butterfly family Lycaenidae appears to be particularly predisposed to cycad‐feeding and several cycadivorous lycaenids are warningly coloured and chemically defended. Cycad–herbivore interactions provide a promising but underutilised study system for investigating plant–insect coevolution, convergent and divergent adaptations, and the multi‐trophic significance of defensive traits; therefore the review ends by suggesting specific research gaps that would be fruitfully addressed in Lepidoptera and other cycad‐feeding insects.
more » « less- Award ID(s):
- 1906333
- PAR ID:
- 10452106
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Ecology Letters
- Volume:
- 23
- Issue:
- 12
- ISSN:
- 1461-023X
- Page Range / eLocation ID:
- p. 1862-1877
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Interconduit pit membranes, which are permeable regions in the primary cell wall that connect to adjacent conduits, play a crucial role in water relations and the movement of nutrients between xylem conduits. However, how pit membrane characteristics might influence water‐carbon coupling remains poorly investigated in cycads. We examined pit characteristics, the anatomical and photosynthetic traits of 13 cycads from a common garden, to determine if pit traits and their coordination are related to water relations and carbon economy. We found that the pit traits of cycads were highly variable and that cycads exhibited a similar tradeoff between pit density and pit area as other plant lineages. Unlike other plant lineages (1) pit membranes, pit apertures, and pit shapes of cycads were not coordinated as in angiosperms; (2) cycads exhibited larger pit membrane areas but lower pit densities relative to ferns and angiosperms, but smaller and similar pit membrane densities to non‐cycad gymnosperms; (3) cycad pit membrane areas and densities were partially coordinated with anatomical traits, with hydraulic supply of the rachis positively coordinated with photosynthesis, whereas pit aperture areas and fractions were negatively coordinated with photosynthetic traits; (4) cycad pit traits reflected adaptation to wetter habitats for Cycadaceae and drier habitats for Zamiaceae. The large variation in pit traits, the unique pit membrane size and density, and the partial coordination of pit traits with anatomical and physiological traits of the rachis and pinna among cycads may have facilitated their dominance in a variety of ecosystems from the Mesozoic to modern times.
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• Drought-induced xylem embolism is a primary cause of plant mortality. Although ~70% of cycads are threatened by extinction and extant cycads diversified during a period of increasing aridification, the vulnerability of cycads to embolism spread has been overlooked. • We quantified the vulnerability to drought-induced embolism, pressure-volume curves, in situ water potentials, and a suite of xylem anatomical traits of leaf pinnae and rachises for 20 cycad species. We tested whether anatomical traits were linked to hydraulic safety in cycads. • Compared to other major vascular plant clades, cycads exhibited similar embolism resistance to angiosperms and pteridophytes but were more vulnerable to embolism than non-cycad gymnosperms. All 20 cycads had both tracheids and vessels, the proportions of which were unrelated to embolism resistance. Only vessel pit membrane fraction was positively correlated to embolism resistance, contrary to angiosperms. Water potential at turgor loss was significantly correlated to embolism resistance among cycads. • Our results show that cycads exhibit low resistance to xylem embolism and that xylem anatomical traits–particularly vessels–may influence embolism resistance together with tracheids. This study highlights the importance of understanding the mechanisms of drought resistance in evolutionarily unique and threatened lineages like the cycads.more » « less
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Summary Drought‐induced xylem embolism is a primary cause of plant mortality. Although
c . 70% of cycads are threatened by extinction and extant cycads diversified during a period of increasing aridification, the vulnerability of cycads to embolism spread has been overlooked.We quantified the vulnerability to drought‐induced embolism, pressure–volume curves,
in situ water potentials, and a suite of xylem anatomical traits of leaf pinnae and rachises for 20 cycad species. We tested whether anatomical traits were linked to hydraulic safety in cycads.Compared with other major vascular plant clades, cycads exhibited similar embolism resistance to angiosperms and pteridophytes but were more vulnerable to embolism than noncycad gymnosperms. All 20 cycads had both tracheids and vessels, the proportions of which were unrelated to embolism resistance. Only vessel pit membrane fraction was positively correlated to embolism resistance, contrary to angiosperms. Water potential at turgor loss was significantly correlated to embolism resistance among cycads.
Our results show that cycads exhibit low resistance to xylem embolism and that xylem anatomical traits – particularly vessels – may influence embolism resistance together with tracheids. This study highlights the importance of understanding the mechanisms of drought resistance in evolutionarily unique and threatened lineages like the cycads.
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Abstract Background and Aims Cycads are a key lineage to understand the early evolution of seed plants and their response to past environmental changes. However, tracing the evolutionary trajectory of cycad species is challenging when the robust relationships at inter- or infrageneric level are not well resolved.
Methods Here, using 2901 single-copy nuclear genes, we explored the species relationships and gene flow within the second largest genus of cycads, i.e. Zamia, based on phylotranscriptomic analyses of 90 % extant Zamia species. Based on a well-resolved phylogenetic framework, we performed gene flow analyses, molecular dating and biogeographical reconstruction to examine the spatiotemporal evolution of Zamia. We also performed ancestral state reconstruction of a total of 62 traits of the genus to comprehensively investigate its morphological evolution.
Key Results Zamia comprises seven major clades corresponding to seven distinct distribution areas in the Americas, with at least three reticulation nodes revealed in this genus. Extant lineages of Zamia initially diversified around 18.4–32.6 (29.14) million years ago in Mega-Mexico, and then expanded eastward into the Caribbean and southward into Central and South America. Ancestral state reconstruction revealed homoplasy in most of the morphological characters.
Conclusions This study revealed congruent phylogenetic relationships from comparative methods/datasets, with some conflicts being the result of incomplete lineage sorting and ancient/recent hybridization events. The strong association between the clades and the biogeographic areas suggested that ancient dispersal events shaped the modern distribution pattern, and regional climatic factors may have resulted in the following in situ diversification. Climate cooling starting during the mid-Miocene is associated with the global expansion of Zamia to tropical South America that has dramatically driven lineage diversification in the New World flora, as well as the extinction of cycad species in the nowadays cooler regions of both hemispheres, as indicated by the fossil records.
