Limits...
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.

Show MeSH

Related in: MedlinePlus

Relationship between ant traits (ant size and recruitment) and the average abundance of extrafloral nectaries (EFNs) and herbivory on plants visited by each ant species.Each point within the graphs represents one ant species (N = 15 ant species). The ant list is presented in decreasing order according to the ant occurrence on EFNs, highlighting the most important ant species in bold and numbered from 1 to 6 in the graphs. A: Smaller ant species generally had higher recruitment than bigger ants (F(1,13) = 3.59; p = 0.06). B: Ant species with lower recruitment generally visited plants with higher amounts of EFNs (F(1,13) = 3.06; p = 0.04). C: Smaller ant species generally visited plants with fewer EFNs (F(1,13) = 2.38; p = 0.055). D: Plants that suffered less damage were generally visited by ants species with higher recruitment (F(1,13) = 3.72; p = 0.06). E: Variation of ant size across ant species was not directly related to herbivory (F(1,13) = 0.32; p = 0.58). All analyses are performed using jackknife procedures.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4401756&req=5

pone.0123806.g004: Relationship between ant traits (ant size and recruitment) and the average abundance of extrafloral nectaries (EFNs) and herbivory on plants visited by each ant species.Each point within the graphs represents one ant species (N = 15 ant species). The ant list is presented in decreasing order according to the ant occurrence on EFNs, highlighting the most important ant species in bold and numbered from 1 to 6 in the graphs. A: Smaller ant species generally had higher recruitment than bigger ants (F(1,13) = 3.59; p = 0.06). B: Ant species with lower recruitment generally visited plants with higher amounts of EFNs (F(1,13) = 3.06; p = 0.04). C: Smaller ant species generally visited plants with fewer EFNs (F(1,13) = 2.38; p = 0.055). D: Plants that suffered less damage were generally visited by ants species with higher recruitment (F(1,13) = 3.72; p = 0.06). E: Variation of ant size across ant species was not directly related to herbivory (F(1,13) = 0.32; p = 0.58). All analyses are performed using jackknife procedures.

Mentions: The four most frequent ant genera on EFNs had different behaviors (described in Nogueira et al. 2012a). Crematogaster was the most active recruiting, followed by Camponotus and Cephalotes, while Pseudomyrmex did not show a clear recruiting behavior. Cephalotes was quite passive in the presence of other insects on plants, while Camponotus were generally very agile, moving fast around nectar resources. Ant traits, EFN abundance and herbivory were functionally related. Smaller ant species generally had higher recruitment than bigger ants (Fig 4A). Ants with lower recruitment and bigger body sizes generally visited plants with higher amounts of nectaries (Fig 4B–4C); and ant recruitment, but not ant size, was negatively related to the average value of foliar herbivory across ant species (Fig 4D–4E), suggesting that the functional relationship between ants and EFNs effectively increases plant resistance against herbivores.


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)

Relationship between ant traits (ant size and recruitment) and the average abundance of extrafloral nectaries (EFNs) and herbivory on plants visited by each ant species.Each point within the graphs represents one ant species (N = 15 ant species). The ant list is presented in decreasing order according to the ant occurrence on EFNs, highlighting the most important ant species in bold and numbered from 1 to 6 in the graphs. A: Smaller ant species generally had higher recruitment than bigger ants (F(1,13) = 3.59; p = 0.06). B: Ant species with lower recruitment generally visited plants with higher amounts of EFNs (F(1,13) = 3.06; p = 0.04). C: Smaller ant species generally visited plants with fewer EFNs (F(1,13) = 2.38; p = 0.055). D: Plants that suffered less damage were generally visited by ants species with higher recruitment (F(1,13) = 3.72; p = 0.06). E: Variation of ant size across ant species was not directly related to herbivory (F(1,13) = 0.32; p = 0.58). All analyses are performed using jackknife procedures.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0123806.g004: Relationship between ant traits (ant size and recruitment) and the average abundance of extrafloral nectaries (EFNs) and herbivory on plants visited by each ant species.Each point within the graphs represents one ant species (N = 15 ant species). The ant list is presented in decreasing order according to the ant occurrence on EFNs, highlighting the most important ant species in bold and numbered from 1 to 6 in the graphs. A: Smaller ant species generally had higher recruitment than bigger ants (F(1,13) = 3.59; p = 0.06). B: Ant species with lower recruitment generally visited plants with higher amounts of EFNs (F(1,13) = 3.06; p = 0.04). C: Smaller ant species generally visited plants with fewer EFNs (F(1,13) = 2.38; p = 0.055). D: Plants that suffered less damage were generally visited by ants species with higher recruitment (F(1,13) = 3.72; p = 0.06). E: Variation of ant size across ant species was not directly related to herbivory (F(1,13) = 0.32; p = 0.58). All analyses are performed using jackknife procedures.
Mentions: The four most frequent ant genera on EFNs had different behaviors (described in Nogueira et al. 2012a). Crematogaster was the most active recruiting, followed by Camponotus and Cephalotes, while Pseudomyrmex did not show a clear recruiting behavior. Cephalotes was quite passive in the presence of other insects on plants, while Camponotus were generally very agile, moving fast around nectar resources. Ant traits, EFN abundance and herbivory were functionally related. Smaller ant species generally had higher recruitment than bigger ants (Fig 4A). Ants with lower recruitment and bigger body sizes generally visited plants with higher amounts of nectaries (Fig 4B–4C); and ant recruitment, but not ant size, was negatively related to the average value of foliar herbivory across ant species (Fig 4D–4E), suggesting that the functional relationship between ants and EFNs effectively increases plant resistance against herbivores.

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