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Geographic mosaic of plant evolution: extrafloral nectary variation mediated by ant and herbivore assemblages.

Nogueira A, Rey PJ, Alcántara JM, Feitosa RM, Lohmann LG - PLoS ONE (2015)

Bottom Line: Studies on this topic could greatly benefit from the general framework of the Geographic Mosaic Theory of Coevolution (GMT).We also did not find significant correlations between EFN traits and ant abundance, herbivory and plant performance across localities.Cases of mismatched and matched populations with the lowest performance were associated with abundant and highly detrimental herbivores.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, São Paulo, Brazil.

ABSTRACT
Herbivory is an ecological process that is known to generate different patterns of selection on defensive plant traits across populations. Studies on this topic could greatly benefit from the general framework of the Geographic Mosaic Theory of Coevolution (GMT). Here, we hypothesize that herbivory represents a strong pressure for extrafloral nectary (EFN) bearing plants, with differences in herbivore and ant visitor assemblages leading to different evolutionary pressures among localities and ultimately to differences in EFN abundance and function. In this study, we investigate this hypothesis by analyzing 10 populations of Anemopaegma album (30 individuals per population) distributed through ca. 600 km of Neotropical savanna and covering most of the geographic range of this plant species. A common garden experiment revealed a phenotypic differentiation in EFN abundance, in which field and experimental plants showed a similar pattern of EFN variation among populations. We also did not find significant correlations between EFN traits and ant abundance, herbivory and plant performance across localities. Instead, a more complex pattern of ant-EFN variation, a geographic mosaic, emerged throughout the geographical range of A. album. We modeled the functional relationship between EFNs and ant traits across ant species and extended this phenotypic interface to characterize local situations of phenotypic matching and mismatching at the population level. Two distinct types of phenotypic matching emerged throughout populations: (1) a population with smaller ants (Crematogaster crinosa) matched with low abundance of EFNs; and (2) seven populations with bigger ants (Camponotus species) matched with higher EFN abundances. Three matched populations showed the highest plant performance and narrower variance of EFN abundance, representing potential plant evolutionary hotspots. Cases of mismatched and matched populations with the lowest performance were associated with abundant and highly detrimental herbivores. Our findings provide insights on the ecology and evolution of plant-ant guarding systems, and suggest new directions to research on facultative mutualistic interactions at wide geographic scales.

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Variation of EFN abundance within and among populations of Anemopaegma album (Mean ± SD).A: EFN variation from field populations of A. album (N = 10 populations; F(9,286) = 14.6; p≤0.001). B: EFN variation of plants grown in common garden (N = 5 populations; F(4,58) = ; p≤0.001). In both cases, we detected differences in the abundance of EFNs among populations, in which Mirangaba had the smallest number of EFNs on the leaflets. Different letters indicate statistical differences in the Tukey post-hoc HSD test (p≤0.05).
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pone.0123806.g003: Variation of EFN abundance within and among populations of Anemopaegma album (Mean ± SD).A: EFN variation from field populations of A. album (N = 10 populations; F(9,286) = 14.6; p≤0.001). B: EFN variation of plants grown in common garden (N = 5 populations; F(4,58) = ; p≤0.001). In both cases, we detected differences in the abundance of EFNs among populations, in which Mirangaba had the smallest number of EFNs on the leaflets. Different letters indicate statistical differences in the Tukey post-hoc HSD test (p≤0.05).

Mentions: All EFN descriptors varied significantly among field populations (EFN abundance: F(9,286) = 14.59, p<0.001; and EFN size: F(9,285) = 14.75, p<0.001). On average, plants from all populations had 41.4 ± 1.6 EFNs per leaflet (means are given ± 1S.E. unless otherwise stated) (S3 Table). The populations from Mirangaba and Caetité had the lowest EFN abundance (3.2 ± 0.4 and 29.6 ± 2.0 EFNs/leaflet, respectively), while Palmeiras and Morro do Chapéu had the highest values (56.7 ± 4.5 and 55.3 ± 2.3, respectively). EFN size varied among populations from 0.15 ± 0.002 mm (Mirangaba) to 0.20 ± 0.003 mm (Morro do Chapéu). The volume of nectar secreted varied from 0.01 to 5.41 μl/plant, and the sugar concentration from 13.7 to 55.6% (S3 Table). EFN traits (size, abundance, and nectar descriptors) did not correlate across populations (r<0.617; p>0.05; N = 10 in the three analyses). In addition, abundance and size of EFNs were not correlated with geographic distance (Mantel r: 0.230 and -0.004, respectively, p>0.17 in both cases). Although plants grown in common garden had fewer EFNs than plants in the field, the pattern of EFN variation in common garden (i.e., under controlled environment) was similar to EFN variation among field populations in the five populations compared (Fig 3).


Geographic mosaic of plant evolution: extrafloral nectary variation mediated by ant and herbivore assemblages.

Nogueira A, Rey PJ, Alcántara JM, Feitosa RM, Lohmann LG - PLoS ONE (2015)

Variation of EFN abundance within and among populations of Anemopaegma album (Mean ± SD).A: EFN variation from field populations of A. album (N = 10 populations; F(9,286) = 14.6; p≤0.001). B: EFN variation of plants grown in common garden (N = 5 populations; F(4,58) = ; p≤0.001). In both cases, we detected differences in the abundance of EFNs among populations, in which Mirangaba had the smallest number of EFNs on the leaflets. Different letters indicate statistical differences in the Tukey post-hoc HSD test (p≤0.05).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4401756&req=5

pone.0123806.g003: Variation of EFN abundance within and among populations of Anemopaegma album (Mean ± SD).A: EFN variation from field populations of A. album (N = 10 populations; F(9,286) = 14.6; p≤0.001). B: EFN variation of plants grown in common garden (N = 5 populations; F(4,58) = ; p≤0.001). In both cases, we detected differences in the abundance of EFNs among populations, in which Mirangaba had the smallest number of EFNs on the leaflets. Different letters indicate statistical differences in the Tukey post-hoc HSD test (p≤0.05).
Mentions: All EFN descriptors varied significantly among field populations (EFN abundance: F(9,286) = 14.59, p<0.001; and EFN size: F(9,285) = 14.75, p<0.001). On average, plants from all populations had 41.4 ± 1.6 EFNs per leaflet (means are given ± 1S.E. unless otherwise stated) (S3 Table). The populations from Mirangaba and Caetité had the lowest EFN abundance (3.2 ± 0.4 and 29.6 ± 2.0 EFNs/leaflet, respectively), while Palmeiras and Morro do Chapéu had the highest values (56.7 ± 4.5 and 55.3 ± 2.3, respectively). EFN size varied among populations from 0.15 ± 0.002 mm (Mirangaba) to 0.20 ± 0.003 mm (Morro do Chapéu). The volume of nectar secreted varied from 0.01 to 5.41 μl/plant, and the sugar concentration from 13.7 to 55.6% (S3 Table). EFN traits (size, abundance, and nectar descriptors) did not correlate across populations (r<0.617; p>0.05; N = 10 in the three analyses). In addition, abundance and size of EFNs were not correlated with geographic distance (Mantel r: 0.230 and -0.004, respectively, p>0.17 in both cases). Although plants grown in common garden had fewer EFNs than plants in the field, the pattern of EFN variation in common garden (i.e., under controlled environment) was similar to EFN variation among field populations in the five populations compared (Fig 3).

Bottom Line: Studies on this topic could greatly benefit from the general framework of the Geographic Mosaic Theory of Coevolution (GMT).We also did not find significant correlations between EFN traits and ant abundance, herbivory and plant performance across localities.Cases of mismatched and matched populations with the lowest performance were associated with abundant and highly detrimental herbivores.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, São Paulo, Brazil.

ABSTRACT
Herbivory is an ecological process that is known to generate different patterns of selection on defensive plant traits across populations. Studies on this topic could greatly benefit from the general framework of the Geographic Mosaic Theory of Coevolution (GMT). Here, we hypothesize that herbivory represents a strong pressure for extrafloral nectary (EFN) bearing plants, with differences in herbivore and ant visitor assemblages leading to different evolutionary pressures among localities and ultimately to differences in EFN abundance and function. In this study, we investigate this hypothesis by analyzing 10 populations of Anemopaegma album (30 individuals per population) distributed through ca. 600 km of Neotropical savanna and covering most of the geographic range of this plant species. A common garden experiment revealed a phenotypic differentiation in EFN abundance, in which field and experimental plants showed a similar pattern of EFN variation among populations. We also did not find significant correlations between EFN traits and ant abundance, herbivory and plant performance across localities. Instead, a more complex pattern of ant-EFN variation, a geographic mosaic, emerged throughout the geographical range of A. album. We modeled the functional relationship between EFNs and ant traits across ant species and extended this phenotypic interface to characterize local situations of phenotypic matching and mismatching at the population level. Two distinct types of phenotypic matching emerged throughout populations: (1) a population with smaller ants (Crematogaster crinosa) matched with low abundance of EFNs; and (2) seven populations with bigger ants (Camponotus species) matched with higher EFN abundances. Three matched populations showed the highest plant performance and narrower variance of EFN abundance, representing potential plant evolutionary hotspots. Cases of mismatched and matched populations with the lowest performance were associated with abundant and highly detrimental herbivores. Our findings provide insights on the ecology and evolution of plant-ant guarding systems, and suggest new directions to research on facultative mutualistic interactions at wide geographic scales.

Show MeSH
Related in: MedlinePlus