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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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Map showing the geographic range of Anemopaegma album (gray) and the location of the ten experimental populations under study.Frequency graphs around the map show the occurrences of ant visitor assemblage at each population, depicted as the percentage of plants occupied by the most important ant genera that fed on EFNs: “Ca.” = Camponotus; “Cr.” = Crematogaster; “Ce.” = Cephalotes; “Ps.” = Pseudomyrmex; “O.” = others ant species (rare species); and “Absent” = proportion of plants without ants. Gray columns represent the frequency of ants at t(0); and black columns represent the frequency of ants at t(1). White columns represent the proportion of unoccupied plants in each population (t(0) and t(1) respectively, see Methods for additional details). The average number of ants per plant in each population is shown for the ant genera with more than 2.5 ants/plant in each population (the average ant abundance here is based on the absolute values without corrections based on plant size). In general, populations with the frequency chart on the right side were the populations with the highest ant visits.
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pone.0123806.g002: Map showing the geographic range of Anemopaegma album (gray) and the location of the ten experimental populations under study.Frequency graphs around the map show the occurrences of ant visitor assemblage at each population, depicted as the percentage of plants occupied by the most important ant genera that fed on EFNs: “Ca.” = Camponotus; “Cr.” = Crematogaster; “Ce.” = Cephalotes; “Ps.” = Pseudomyrmex; “O.” = others ant species (rare species); and “Absent” = proportion of plants without ants. Gray columns represent the frequency of ants at t(0); and black columns represent the frequency of ants at t(1). White columns represent the proportion of unoccupied plants in each population (t(0) and t(1) respectively, see Methods for additional details). The average number of ants per plant in each population is shown for the ant genera with more than 2.5 ants/plant in each population (the average ant abundance here is based on the absolute values without corrections based on plant size). In general, populations with the frequency chart on the right side were the populations with the highest ant visits.

Mentions: Plants of A. album occur throughout the Brazilian states of Minas Gerais and Bahia (Fig 2), where they inhabit ‘cerrados’, ‘caatingas’, and transitional habitats known as ‘carrascos’. The climate is seasonal with temperatures ranging between 20.3° and 31°C in the rainy season and between 15.3° and 30.5°C in the dry season. The mean annual rainfall varies among localities between 650 mm in the north and 1.100 mm in the south, with accumulated mean rainfall in the rainy season around 710 mm (November–February) and around 40 mm (June–August) in the dry season.


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)

Map showing the geographic range of Anemopaegma album (gray) and the location of the ten experimental populations under study.Frequency graphs around the map show the occurrences of ant visitor assemblage at each population, depicted as the percentage of plants occupied by the most important ant genera that fed on EFNs: “Ca.” = Camponotus; “Cr.” = Crematogaster; “Ce.” = Cephalotes; “Ps.” = Pseudomyrmex; “O.” = others ant species (rare species); and “Absent” = proportion of plants without ants. Gray columns represent the frequency of ants at t(0); and black columns represent the frequency of ants at t(1). White columns represent the proportion of unoccupied plants in each population (t(0) and t(1) respectively, see Methods for additional details). The average number of ants per plant in each population is shown for the ant genera with more than 2.5 ants/plant in each population (the average ant abundance here is based on the absolute values without corrections based on plant size). In general, populations with the frequency chart on the right side were the populations with the highest ant visits.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0123806.g002: Map showing the geographic range of Anemopaegma album (gray) and the location of the ten experimental populations under study.Frequency graphs around the map show the occurrences of ant visitor assemblage at each population, depicted as the percentage of plants occupied by the most important ant genera that fed on EFNs: “Ca.” = Camponotus; “Cr.” = Crematogaster; “Ce.” = Cephalotes; “Ps.” = Pseudomyrmex; “O.” = others ant species (rare species); and “Absent” = proportion of plants without ants. Gray columns represent the frequency of ants at t(0); and black columns represent the frequency of ants at t(1). White columns represent the proportion of unoccupied plants in each population (t(0) and t(1) respectively, see Methods for additional details). The average number of ants per plant in each population is shown for the ant genera with more than 2.5 ants/plant in each population (the average ant abundance here is based on the absolute values without corrections based on plant size). In general, populations with the frequency chart on the right side were the populations with the highest ant visits.
Mentions: Plants of A. album occur throughout the Brazilian states of Minas Gerais and Bahia (Fig 2), where they inhabit ‘cerrados’, ‘caatingas’, and transitional habitats known as ‘carrascos’. The climate is seasonal with temperatures ranging between 20.3° and 31°C in the rainy season and between 15.3° and 30.5°C in the dry season. The mean annual rainfall varies among localities between 650 mm in the north and 1.100 mm in the south, with accumulated mean rainfall in the rainy season around 710 mm (November–February) and around 40 mm (June–August) in the dry season.

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