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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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Matched and mismatched populations based on the local association between the community-level ant traits and the average values of EFN abundance.A-B: We used the phenotypic interface (or functional models) based on the relationship previously described between EFN abundance and ant traits across ant-species (Fig 4B–4C, and here highlighted in orange) in order to position the average values of EFNs and the community-level ant traits of each population. With this procedure, we were able to classify objectively each population in phenotypic matching and mismatching cases. Based on EFN abundance and community-level ant-recruitment (A) four populations were classified as mismatched populations. Based on EFN abundance and community-level ant-size (B) two populations, positioned outside the confidence interval (dashed orange lines), were classified as mismatched populations. C-D: The frequency of occupied plants (and the average ant abundance) was not clearly associated with the average EFN abundance, but confirmed the expected pattern of matched populations classified by community-level ant size and EFNs (evidenced by the gray region).
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pone.0123806.g005: Matched and mismatched populations based on the local association between the community-level ant traits and the average values of EFN abundance.A-B: We used the phenotypic interface (or functional models) based on the relationship previously described between EFN abundance and ant traits across ant-species (Fig 4B–4C, and here highlighted in orange) in order to position the average values of EFNs and the community-level ant traits of each population. With this procedure, we were able to classify objectively each population in phenotypic matching and mismatching cases. Based on EFN abundance and community-level ant-recruitment (A) four populations were classified as mismatched populations. Based on EFN abundance and community-level ant-size (B) two populations, positioned outside the confidence interval (dashed orange lines), were classified as mismatched populations. C-D: The frequency of occupied plants (and the average ant abundance) was not clearly associated with the average EFN abundance, but confirmed the expected pattern of matched populations classified by community-level ant size and EFNs (evidenced by the gray region).

Mentions: No clear correlation emerged across populations between ant functional traits and EFN abundance (three descriptors), size or nectar secretion (r < 0.61; N = 10; p<0.05 in all cases). More specifically, community-level ant size and recruitment were not correlated with EFN abundance at the base of leaflets (Fig 5A–5B). We also examined a more complex scenario of phenotypic matching and mismatching of A. album with their local ant visitor assemblages. We positioned each locality on the phenotype-function relationships between ant traits and EFN abundance (Fig 4B–4C; note that the regression lines and their confidence intervals in the Fig 5A–5B are the same depicted in Fig 4B–4C). Four populations were distant from the expected line depicted between EFN abundance and community-level ant recruitment (Fig 5A), and represent cases of phenotypic mismatching for this ant-plant trait combination. At least two of these populations, Grão Mogol and Morro do Chapéu, showed some of the highest values of ant abundance (4.9 and 5.6 ants/plant, respectively; Fig 5C–5D) and lowest herbivore damage (27.3 and 16.7%, respectively).


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)

Matched and mismatched populations based on the local association between the community-level ant traits and the average values of EFN abundance.A-B: We used the phenotypic interface (or functional models) based on the relationship previously described between EFN abundance and ant traits across ant-species (Fig 4B–4C, and here highlighted in orange) in order to position the average values of EFNs and the community-level ant traits of each population. With this procedure, we were able to classify objectively each population in phenotypic matching and mismatching cases. Based on EFN abundance and community-level ant-recruitment (A) four populations were classified as mismatched populations. Based on EFN abundance and community-level ant-size (B) two populations, positioned outside the confidence interval (dashed orange lines), were classified as mismatched populations. C-D: The frequency of occupied plants (and the average ant abundance) was not clearly associated with the average EFN abundance, but confirmed the expected pattern of matched populations classified by community-level ant size and EFNs (evidenced by the gray region).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0123806.g005: Matched and mismatched populations based on the local association between the community-level ant traits and the average values of EFN abundance.A-B: We used the phenotypic interface (or functional models) based on the relationship previously described between EFN abundance and ant traits across ant-species (Fig 4B–4C, and here highlighted in orange) in order to position the average values of EFNs and the community-level ant traits of each population. With this procedure, we were able to classify objectively each population in phenotypic matching and mismatching cases. Based on EFN abundance and community-level ant-recruitment (A) four populations were classified as mismatched populations. Based on EFN abundance and community-level ant-size (B) two populations, positioned outside the confidence interval (dashed orange lines), were classified as mismatched populations. C-D: The frequency of occupied plants (and the average ant abundance) was not clearly associated with the average EFN abundance, but confirmed the expected pattern of matched populations classified by community-level ant size and EFNs (evidenced by the gray region).
Mentions: No clear correlation emerged across populations between ant functional traits and EFN abundance (three descriptors), size or nectar secretion (r < 0.61; N = 10; p<0.05 in all cases). More specifically, community-level ant size and recruitment were not correlated with EFN abundance at the base of leaflets (Fig 5A–5B). We also examined a more complex scenario of phenotypic matching and mismatching of A. album with their local ant visitor assemblages. We positioned each locality on the phenotype-function relationships between ant traits and EFN abundance (Fig 4B–4C; note that the regression lines and their confidence intervals in the Fig 5A–5B are the same depicted in Fig 4B–4C). Four populations were distant from the expected line depicted between EFN abundance and community-level ant recruitment (Fig 5A), and represent cases of phenotypic mismatching for this ant-plant trait combination. At least two of these populations, Grão Mogol and Morro do Chapéu, showed some of the highest values of ant abundance (4.9 and 5.6 ants/plant, respectively; Fig 5C–5D) and lowest herbivore damage (27.3 and 16.7%, respectively).

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