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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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Related in: MedlinePlus

The average values of herbivory and three fitness descriptors per population were used to characterize the potential effect of ants on plants.Note the position of the three populations considered plant-evolutionary hotspots, in which the EFN—ant association could have a positive effect to the plants, decreasing herbivory and increasing fitness: Mirangaba (mi), Morro do Chapéu (mc) and Grão Mogol (gm). Solid and dashed lines had different levels of significance (p<0.05 and p<0.10, respectively).
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pone.0123806.g006: The average values of herbivory and three fitness descriptors per population were used to characterize the potential effect of ants on plants.Note the position of the three populations considered plant-evolutionary hotspots, in which the EFN—ant association could have a positive effect to the plants, decreasing herbivory and increasing fitness: Mirangaba (mi), Morro do Chapéu (mc) and Grão Mogol (gm). Solid and dashed lines had different levels of significance (p<0.05 and p<0.10, respectively).

Mentions: There was no significant correlation among EFN traits and the descriptors of plant performance across populations (Table 2). In contrast, a significant relationship was found among average abundance of ants, some descriptors of plant performance, and community-level ant traits (Table 2 and Fig 6). In general, the higher the ant abundance, the higher the production of leaves and the proportion of flowering plants across populations (Fig 6C–6E). Populations with higher abundances of ants also showed smaller community-level ant size and higher community-level ant recruitment (Table 2). Moreover, the three descriptors of plant performance were also positively correlated with each other (Table 2).


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)

The average values of herbivory and three fitness descriptors per population were used to characterize the potential effect of ants on plants.Note the position of the three populations considered plant-evolutionary hotspots, in which the EFN—ant association could have a positive effect to the plants, decreasing herbivory and increasing fitness: Mirangaba (mi), Morro do Chapéu (mc) and Grão Mogol (gm). Solid and dashed lines had different levels of significance (p<0.05 and p<0.10, respectively).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0123806.g006: The average values of herbivory and three fitness descriptors per population were used to characterize the potential effect of ants on plants.Note the position of the three populations considered plant-evolutionary hotspots, in which the EFN—ant association could have a positive effect to the plants, decreasing herbivory and increasing fitness: Mirangaba (mi), Morro do Chapéu (mc) and Grão Mogol (gm). Solid and dashed lines had different levels of significance (p<0.05 and p<0.10, respectively).
Mentions: There was no significant correlation among EFN traits and the descriptors of plant performance across populations (Table 2). In contrast, a significant relationship was found among average abundance of ants, some descriptors of plant performance, and community-level ant traits (Table 2 and Fig 6). In general, the higher the ant abundance, the higher the production of leaves and the proportion of flowering plants across populations (Fig 6C–6E). Populations with higher abundances of ants also showed smaller community-level ant size and higher community-level ant recruitment (Table 2). Moreover, the three descriptors of plant performance were also positively correlated with each other (Table 2).

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