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

Ant—plant—herbivore system in a Neotropical savanna.A: Adult plant of A. album with immature fruits. B: Plant with nearly no leaf damage. C: Plant with severe leaf damage. D-E: Leaflets from different individuals of A. album showing wide variation in the number of EFNs on the base of leaflets (foliar cluster of EFNs). F-H: Most damaging herbivores for A. album: cricket Xestotrachelus robustus, and the beetles Charidotis sp. and Sumitrosis sp. I-L: Common ant species that visited EFNs, including four of the six most frequent ant species. Scale bars represent 1 mm in ant images; ant images are available in its original version in the AntWeb page (photo A. Nobile).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0123806.g001: Ant—plant—herbivore system in a Neotropical savanna.A: Adult plant of A. album with immature fruits. B: Plant with nearly no leaf damage. C: Plant with severe leaf damage. D-E: Leaflets from different individuals of A. album showing wide variation in the number of EFNs on the base of leaflets (foliar cluster of EFNs). F-H: Most damaging herbivores for A. album: cricket Xestotrachelus robustus, and the beetles Charidotis sp. and Sumitrosis sp. I-L: Common ant species that visited EFNs, including four of the six most frequent ant species. Scale bars represent 1 mm in ant images; ant images are available in its original version in the AntWeb page (photo A. Nobile).

Mentions: Anemopaegma album (Bignoniaceae) is a bee-pollinated and wind-dispersed [32] shrub (Fig 1A), with 3-foliolated leaves and large quantitative variation in extrafloral nectaries (EFNs) on leaflets. The EFNs are patteliform glandular trichomes that are mostly grouped at the base of the abaxial side of leaflets (Fig 1D–1E), and rarely sparsely distributed over the abaxial and adaxial leaflet blades. EFN abundance is positively related to ant visitor abundance [33]. At least three insect herbivores (Coleoptera and Orthoptera) feed on leaf tissues causing extreme foliage loss (Fig 1B–1C), while two caterpillars feed on flowers and fruits (A. Nogueira, pers.obs.).


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)

Ant—plant—herbivore system in a Neotropical savanna.A: Adult plant of A. album with immature fruits. B: Plant with nearly no leaf damage. C: Plant with severe leaf damage. D-E: Leaflets from different individuals of A. album showing wide variation in the number of EFNs on the base of leaflets (foliar cluster of EFNs). F-H: Most damaging herbivores for A. album: cricket Xestotrachelus robustus, and the beetles Charidotis sp. and Sumitrosis sp. I-L: Common ant species that visited EFNs, including four of the six most frequent ant species. Scale bars represent 1 mm in ant images; ant images are available in its original version in the AntWeb page (photo A. Nobile).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0123806.g001: Ant—plant—herbivore system in a Neotropical savanna.A: Adult plant of A. album with immature fruits. B: Plant with nearly no leaf damage. C: Plant with severe leaf damage. D-E: Leaflets from different individuals of A. album showing wide variation in the number of EFNs on the base of leaflets (foliar cluster of EFNs). F-H: Most damaging herbivores for A. album: cricket Xestotrachelus robustus, and the beetles Charidotis sp. and Sumitrosis sp. I-L: Common ant species that visited EFNs, including four of the six most frequent ant species. Scale bars represent 1 mm in ant images; ant images are available in its original version in the AntWeb page (photo A. Nobile).
Mentions: Anemopaegma album (Bignoniaceae) is a bee-pollinated and wind-dispersed [32] shrub (Fig 1A), with 3-foliolated leaves and large quantitative variation in extrafloral nectaries (EFNs) on leaflets. The EFNs are patteliform glandular trichomes that are mostly grouped at the base of the abaxial side of leaflets (Fig 1D–1E), and rarely sparsely distributed over the abaxial and adaxial leaflet blades. EFN abundance is positively related to ant visitor abundance [33]. At least three insect herbivores (Coleoptera and Orthoptera) feed on leaf tissues causing extreme foliage loss (Fig 1B–1C), while two caterpillars feed on flowers and fruits (A. Nogueira, pers.obs.).

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