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Convergent Evolution towards High Net Carbon Gain Efficiency Contributes to the Shade Tolerance of Palms (Arecaceae).

ABSTRACT: Most palm species occur in the shaded lower strata of tropical rain forests, but how their traits relate to shade adaptation is poorly understood. We hypothesized that palms are adapted to the shade of their native habitats by convergent evolution towards high net carbon gain efficiency (CGEn), which is given by the maximum photosynthetic rate to dark respiration rate ratio. Leaf mass per area, maximum photosynthetic rate, dark respiration and N and P concentrations were measured in 80 palm species grown in a common garden, and combined with data of 30 palm species growing in their native habitats. Compared to other species from the global leaf economics data, dicotyledonous broad-leaved trees in tropical rainforest or other monocots in the global leaf economics data, palms possessed consistently higher CGEn, achieved by lowered dark respiration and fairly high foliar P concentration. Combined phylogenetic analyses of evolutionary signal and trait evolution revealed convergent evolution towards high CGEn in palms. We conclude that high CGEn is an evolutionary strategy that enables palms to better adapt to shady environments than coexisting dicot tree species, and may convey advantages in competing with them in the tropical forest understory. These findings provide important insights for understanding the evolution and ecology of palms, and for understanding plant shade adaptations of lower rainforest strata. Moreover, given the dominant role of palms in tropical forests, these findings are important for modelling carbon and nutrient cycling in tropical forest ecosystems.

SUBMITTER: Ma RY

PROVIDER: S-EPMC4604201 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Convergent Evolution towards High Net Carbon Gain Efficiency Contributes to the Shade Tolerance of Palms (Arecaceae).

Ma Ren-Yi RY Zhang Jiao-Lin JL Cavaleri Molly A MA Sterck Frank F Strijk Joeri S JS Cao Kun-Fang KF

PloS one 20151013 10

Most palm species occur in the shaded lower strata of tropical rain forests, but how their traits relate to shade adaptation is poorly understood. We hypothesized that palms are adapted to the shade of their native habitats by convergent evolution towards high net carbon gain efficiency (CGEn), which is given by the maximum photosynthetic rate to dark respiration rate ratio. Leaf mass per area, maximum photosynthetic rate, dark respiration and N and P concentrations were measured in 80 palm spec ...[more]

PMID: 26461108

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Project description:Background and aimsThe Arecoideae is the largest and most diverse of the five subfamilies of palms (Arecaceae/Palmae), containing >50 % of the species in the family. Despite its importance, phylogenetic relationships among Arecoideae are poorly understood. Here the most densely sampled phylogenetic analysis of Arecoideae available to date is presented. The results are used to test the current classification of the subfamily and to identify priority areas for future research.MethodsDNA sequence data for the low-copy nuclear genes PRK and RPB2 were collected from 190 palm species, covering 103 (96 %) genera of Arecoideae. The data were analysed using the parsimony ratchet, maximum likelihood, and both likelihood and parsimony bootstrapping.Key results and conclusionsDespite the recovery of paralogues and pseudogenes in a small number of taxa, PRK and RPB2 were both highly informative, producing well-resolved phylogenetic trees with many nodes well supported by bootstrap analyses. Simultaneous analyses of the combined data sets provided additional resolution and support. Two areas of incongruence between PRK and RPB2 were strongly supported by the bootstrap relating to the placement of tribes Chamaedoreeae, Iriarteeae and Reinhardtieae; the causes of this incongruence remain uncertain. The current classification within Arecoideae was strongly supported by the present data. Of the 14 tribes and 14 sub-tribes in the classification, only five sub-tribes from tribe Areceae (Basseliniinae, Linospadicinae, Oncospermatinae, Rhopalostylidinae and Verschaffeltiinae) failed to receive support. Three major higher level clades were strongly supported: (1) the RRC clade (Roystoneeae, Reinhardtieae and Cocoseae), (2) the POS clade (Podococceae, Oranieae and Sclerospermeae) and (3) the core arecoid clade (Areceae, Euterpeae, Geonomateae, Leopoldinieae, Manicarieae and Pelagodoxeae). However, new data sources are required to elucidate ambiguities that remain in phylogenetic relationships among and within the major groups of Arecoideae, as well as within the Areceae, the largest tribe in the palm family.

Project description:Pollination of Neotropical dioecious trees is commonly related to generalist insects. Similar data for non-tree species with separated genders are inconclusive. Recent studies on pollination of dioecious Chamaedorea palms (Arecaceae) suggest that species are either insect- or wind-pollinated. However, the wide variety of inflorescence and floral attributes within the genus suggests mixed pollination mode involving entomophily and anemophily. To evaluate this hypothesis, we studied the pollination of Chamaedorea costaricana, C. macrospadix, C. pinnatifrons and C. tepejilote in two montane forests in Costa Rica. A complementary morphological analysis of floral traits was carried out to distinguish species groups within the genus according to their most probable pollination mechanism. We conducted pollinator exclusion experiments, field observations on visitors to pistillate and staminate inflorescences, and trapped airborne pollen. A cluster analysis using 18 floral traits selected for their association with wind and insect pollination syndromes was carried out using 52 Chamaedorea species. Exclusion experiments showed that both wind and insects, mostly thrips (Thysanoptera), pollinated the studied species. Thrips used staminate inflorescences as brood sites and pollinated pistillate flowers by deception. Insects caught on pistillate inflorescences transported pollen, while traps proved that pollen is wind-borne. Our empirical findings clearly suggest that pollination of dioecious Chamaedorea palms is likely to involve both insects and wind. A cluster analysis showed that the majority of studied species have a combination of floral traits that allow for both pollination modes. Our pollination experiments and morphological analysis both suggest that while some species may be completely entomophilous or anemophilous, ambophily might be a common condition within Chamaedorea. Our results propose a higher diversity of pollination mechanisms of Neotropical dioecious species than previously suggested.

Project description:Background and aimsA long-running debate centres on whether shade tolerance of tree seedlings is mainly a function of traits maximizing net carbon gain in low light, or of traits minimizing carbon loss. To test these alternatives, leaf display, light-interception efficiency, and simulated net daily carbon gain of juvenile temperate evergreens of differing shade tolerance were measured, and how these variables are influenced by ontogeny was queried.MethodsThe biomass distribution of juveniles (17-740 mm tall) of seven temperate rainforest evergreens growing in low (approx. 4 %) light in the understorey of a second-growth stand was quantified. Daytime and night-time gas exchange rates of leaves were also determined, and crown architecture was recorded digitally. YPLANT was used to model light interception and carbon gain.ResultsAn index of species shade tolerance correlated closely with photosynthetic capacities and respiration rates per unit mass of leaves, but only weakly with respiration per unit area. Accumulation of many leaf cohorts by shade-tolerant species meant that their ratios of foliage area to biomass (LAR) decreased more gradually with ontogeny than those of light-demanders, but also increased self-shading; this depressed the foliage silhouette-to-area ratio (STAR), which was used as an index of light-interception efficiency. As a result, displayed leaf area ratio (LAR(d) = LAR × STAR) of large seedlings was not related to species shade tolerance. Self-shading also caused simulated net daily carbon assimilation rates of shade-tolerant species to decrease with ontogeny, leading to a negative correlation of shade tolerance with net daily carbon gain of large (500 mm tall) seedlings in the understorey.ConclusionsThe results suggest that efficiency of energy capture is not an important correlate of shade tolerance in temperate rainforest evergreens. Ontogenetic increases in self-shading largely nullify the potential carbon gain advantages expected to result from low respiration rates and long leaf lifespans in shade-tolerant evergreens. The main advantage of their long-lived leaves is probably in reducing the costs of crown maintenance.

Project description:BACKGROUND AND AIMS: Molecular phylogenetic studies of palms (Arecaceae) have not yet provided a fully resolved phylogeny of the family. There is a need to increase the current set of markers to resolve difficult groups such as the Neotropical subtribe Bactridinae (Arecoideae: Cocoseae). We propose the use of two single-copy nuclear genes as valuable tools for palm phylogenetics. METHODS: New primers were developed for the amplification of the AGAMOUS 1 (AG1) and PHYTOCHROME B (PHYB) genes. For the AGAMOUS gene, the paralogue 1 of Elaeis guineensis (EgAG1) was targeted. The region amplified contained coding sequences between the MIKC K and C MADS-box domains. For the PHYB gene, exon 1 (partial sequence) was first amplified in palm species using published degenerate primers for Poaceae, and then specific palm primers were designed. The two gene portions were sequenced in 22 species of palms representing all genera of Bactridinae, with emphasis on Astrocaryum and Hexopetion, the status of the latter genus still being debated. KEY RESULTS: The new primers designed allow consistent amplification and high-quality sequencing within the palm family. The two loci studied produced more variability than chloroplast loci and equally or less variability than PRK, RPBII and ITS nuclear markers. The phylogenetic structure obtained with AG1 and PHYB genes provides new insights into intergeneric relationships within the Bactridinae and the intrageneric structure of Astrocaryum. The Hexopetion clade was recovered as monophyletic with both markers and was weakly supported as sister to Astrocaryum sensu stricto in the combined analysis. The rare Astrocaryum minus formed a species complex with Astrocaryum gynacanthum. Moreover, both AG1 and PHYB contain a microsatellite that could have further uses in species delimitation and population genetics. CONCLUSIONS: AG1 and PHYB provide additional phylogenetic information within the palm family, and should prove useful in combination with other genes to improve the resolution of palm phylogenies.

Dataset Information

Convergent Evolution towards High Net Carbon Gain Efficiency Contributes to the Shade Tolerance of Palms (Arecaceae).

Publications

Convergent Evolution towards High Net Carbon Gain Efficiency Contributes to the Shade Tolerance of Palms (Arecaceae).

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