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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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Standardized variation of EFN abundance within populations of A. album.Variance comparisons revealed two major groups with distinct patterns of EFN variance: (1) five populations on the left side with larger variances, and (2) the other four populations with narrower variances. The Mirangaba population appears differently from all other populations, with a narrower EFN variance. Three plant-evolutionary hotspots (matching populations with higher performance and narrower EFN variance) are highlighted in gray: Grão Mogol, Morro do Chapéu and Mirangaba. Asterisks indicate mismatched populations. Different letters indicate statistical differences among population variances (p≤0.05).
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pone.0123806.g007: Standardized variation of EFN abundance within populations of A. album.Variance comparisons revealed two major groups with distinct patterns of EFN variance: (1) five populations on the left side with larger variances, and (2) the other four populations with narrower variances. The Mirangaba population appears differently from all other populations, with a narrower EFN variance. Three plant-evolutionary hotspots (matching populations with higher performance and narrower EFN variance) are highlighted in gray: Grão Mogol, Morro do Chapéu and Mirangaba. Asterisks indicate mismatched populations. Different letters indicate statistical differences among population variances (p≤0.05).

Mentions: Few populations among those identified as phenotypically matched with their local ant assemblages had both high average values of plant performance and low variance of EFN abundance, and therefore are considered potential plant evolutionary hotspots (see Methods): Mirangaba, Morro do Chapéu, and to a lesser extent Grão Mogol. These three populations had higher values of ant abundance per plant (Fig 5D) and positive values of relative leaf production (Fig 6C–6D). In particular, Mirangaba was the population in which all descriptors of performance scored maximum values, with the minimum average values of herbivory, and the minimum variance of EFN abundance (Fig 7). Morro do Chapéu showed low levels of herbivory and high average values of at least two of the three performance descriptors (i.e., relative production of leaves and proportion of flowering plants). Grão Mogol showed a less clear pattern, with intermediate values of herbivory and high relative production of leaves (Fig 6). Grão Mogol and Morro do Chapéu had similar EFN variance that was greater than the variance on Mirangaba (Fig 7), but smaller than the other five populations. While the evolutionary hotspots Morro do Chapéu and Grão Mogol were driven by relatively large Camponotus ants, the Mirangaba hotspot was driven by small Crematogaster ants (Figs 2 and 5B).


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)

Standardized variation of EFN abundance within populations of A. album.Variance comparisons revealed two major groups with distinct patterns of EFN variance: (1) five populations on the left side with larger variances, and (2) the other four populations with narrower variances. The Mirangaba population appears differently from all other populations, with a narrower EFN variance. Three plant-evolutionary hotspots (matching populations with higher performance and narrower EFN variance) are highlighted in gray: Grão Mogol, Morro do Chapéu and Mirangaba. Asterisks indicate mismatched populations. Different letters indicate statistical differences among population variances (p≤0.05).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0123806.g007: Standardized variation of EFN abundance within populations of A. album.Variance comparisons revealed two major groups with distinct patterns of EFN variance: (1) five populations on the left side with larger variances, and (2) the other four populations with narrower variances. The Mirangaba population appears differently from all other populations, with a narrower EFN variance. Three plant-evolutionary hotspots (matching populations with higher performance and narrower EFN variance) are highlighted in gray: Grão Mogol, Morro do Chapéu and Mirangaba. Asterisks indicate mismatched populations. Different letters indicate statistical differences among population variances (p≤0.05).
Mentions: Few populations among those identified as phenotypically matched with their local ant assemblages had both high average values of plant performance and low variance of EFN abundance, and therefore are considered potential plant evolutionary hotspots (see Methods): Mirangaba, Morro do Chapéu, and to a lesser extent Grão Mogol. These three populations had higher values of ant abundance per plant (Fig 5D) and positive values of relative leaf production (Fig 6C–6D). In particular, Mirangaba was the population in which all descriptors of performance scored maximum values, with the minimum average values of herbivory, and the minimum variance of EFN abundance (Fig 7). Morro do Chapéu showed low levels of herbivory and high average values of at least two of the three performance descriptors (i.e., relative production of leaves and proportion of flowering plants). Grão Mogol showed a less clear pattern, with intermediate values of herbivory and high relative production of leaves (Fig 6). Grão Mogol and Morro do Chapéu had similar EFN variance that was greater than the variance on Mirangaba (Fig 7), but smaller than the other five populations. While the evolutionary hotspots Morro do Chapéu and Grão Mogol were driven by relatively large Camponotus ants, the Mirangaba hotspot was driven by small Crematogaster ants (Figs 2 and 5B).

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