In the formation of species, adaptation by natural selection generates distinct combinations of traits that function well together. The maintenance of adaptive trait combinations in the face of gene flow depends on the strength and nature of selection acting on the underlying genetic loci. Floral pollination syndromes exemplify the evolution of trait combinations adaptive for particular pollinators. The North American wildflower genus
Combinations of correlated floral traits have arisen repeatedly across angiosperms through convergent evolution in response to pollinator selection to optimize reproduction. While some plant groups exhibit very distinct combinations of traits adapted to specific pollinators (so-called pollination syndromes), others do not. Determining how floral traits diverge across clades and whether floral traits show predictable correlations in diverse groups of flowering plants is key to determining the extent to which pollinator-mediated selection drives diversification. The North American
- Award ID(s):
- 1757780
- NSF-PAR ID:
- 10505825
- Publisher / Repository:
- Frontiers Media
- Date Published:
- Journal Name:
- Frontiers in Plant Science
- Volume:
- 13
- ISSN:
- 1664-462X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Barton, Nick H. (Ed.)more » « less
Penstemon displays remarkable floral syndrome convergence, with at least 20 separate lineages that have evolved from ancestral bee pollination syndrome (wide blue-purple flowers that present a landing platform for bees and small amounts of nectar) to hummingbird pollination syndrome (bright red narrowly tubular flowers offering copious nectar). Related taxa that differ in floral syndrome offer an attractive opportunity to examine the genomic basis of complex trait divergence. In this study, we characterized genomic divergence among 229 individuals from aPenstemon species complex that includes both bee and hummingbird floral syndromes. Field plants are easily classified into species based on phenotypic differences and hybrids displaying intermediate floral syndromes are rare. Despite unambiguous phenotypic differences, genome-wide differentiation between species is minimal. Hummingbird-adapted populations are more genetically similar to nearby bee-adapted populations than to geographically distant hummingbird-adapted populations, in terms of genome-wided XY . However, a small number of genetic loci are strongly differentiated between species. These approximately 20 “species-diagnostic loci,” which appear to have nearly fixed differences between pollination syndromes, are sprinkled throughout the genome in high recombination regions. Several map closely to previously established floral trait quantitative trait loci (QTLs). The striking difference between the diagnostic loci and the genome as whole suggests strong selection to maintain distinct combinations of traits, but with sufficient gene flow to homogenize the genomic background. A surprisingly small number of alleles confer phenotypic differences that form the basis of species identity in this species complex. -
In the formation of species, adaptation by natural selection generates distinct combinations of traits that function well together. The maintenance of adaptive trait combinations in the face of gene flow depends on the strength and nature of selection acting on the underlying genetic loci. Floral pollination syndromes exemplify the evolution of trait combinations adaptive for particular pollinators. The North American wildflower genus Penstemon displays remarkable floral syndrome convergence, with at least 20 separate lineages that have evolved from ancestral bee pollination syndrome (wide blue-purple flowers that present a landing platform for bees and small amounts of nectar) to hummingbird pollination syndrome (bright red narrowly tubular flowers offering copious nectar). Related taxa that differ in floral syndrome offer an attractive opportunity to examine the genomic basis of complex trait divergence. In this study, we characterized genomic divergence among 229 individuals from a Penstemon species complex that includes both bee and hummingbird floral syndromes. Field plants are easily classified into species based on phenotypic differences and hybrids displaying intermediate floral syndromes are rare. Despite unambiguous phenotypic differences, genomewide differentiation between species is minimal. Hummingbird-adapted populations are more genetically similar to nearby bee-adapted populations than to geographically distant hummingbird-adapted populations, in terms of genomewide dXY. However, a small number of genetic loci are strongly differentiated between species. These ~ 20 "species-diagnostic loci", which appear to have nearly fixed differences between pollination syndromes, are sprinkled throughout the genome in high recombination regions. Several map closely to previously established floral trait QTLs. The striking difference between the diagnostic loci and the genome as whole suggests strong selection to maintain distinct combinations of traits, but with sufficient gene flow to homogenize the genomic background. A surprisingly small number of alleles confer phenotypic differences that form the basis of species identity in this species complex.more » « less
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Abstract Different populations of plant species can adapt to their local pollinators and diverge in floral traits accordingly. Floral traits are subject to pollinator‐driven natural selection to enhance plant reproductive success. Studies on temperate plant systems have shown pollinator‐driven selection results in floral trait variation along elevational gradients, but studies in tropical systems are lacking. We analyzed floral traits and pollinator assemblages in the Neotropical bee‐pollinated taxon
Costus guanaiensis var.tarmicus across four sites along a steep elevational gradient in Peru. We found variations in floral traits of size, color, and reward, and in the pollinator assemblage along the elevational gradient. We examined our results considering two hypotheses, (1) local adaptation to different bee assemblages, and (2) the early stages of an evolutionary shift to a new pollinator functional group (hummingbirds). We found some evidence consistent with the adaptation ofC. guanaiensis var.tarmicus to the local bee fauna along the studied elevational gradient. Corolla width across sites was associated with bee thorax width of the local most frequent pollinator. However, we could not rule out the possibility of the beginning of a bee‐to‐hummingbird pollination shift in the highest‐studied site. Our study is one of the few geographic‐scale analyses of floral trait and pollinator assemblage variation in tropical plant species. Our results broaden our understanding of plant‐pollinator interactions beyond temperate systems by showing substantial intraspecific divergence in both floral traits and pollinator assemblages across geographic space in a tropical plant species. -
Different populations of plant species can adapt to their local pollinators and diverge in floral traits accordingly. Floral traits are subject to pollinator-driven natural selection to enhance plant reproductive success. Studies on temperate plant systems have shown pollinator-driven selection results in floral trait variation along elevational gradients, but studies in tropical systems are lacking. We analyzed floral traits and pollinator assemblages in the Neotropical bee-pollinated taxon Costus guanaiensis var. tarmicus across four sites along a steep elevational gradient in Peru. We found variations in floral traits of size, color, and reward, and in the pollinator assemblage along the elevational gradient. We examined our results considering two hypotheses, (1) local adaptation to different bee assemblages, and (2) the early stages of an evolutionary shift to a new pollinator functional group (hummingbirds). We found some evidence consistent with the adaptation of C. guanaiensis var. tarmicus to the local bee fauna along the studied elevational gradient. Corolla width across sites was associated with bee thorax width of the local most frequent pollinator. However, we could not rule out the possibility of the beginning of a bee-to-hummingbird pollination shift in the highest-studied site. Our study is one of the few geographic-scale analyses of floral trait and pollinator assemblage variation in tropical plant species. Our results broaden our understanding of plant-pollinator interactions beyond temperate systems by showing substantial intraspecific divergence in both floral traits and pollinator assemblages across geographic space in a tropical plant species.more » « less
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Premise Closely related plant species with overlapping ranges often experience competition for pollination services. Such competition can select for divergence in floral traits that attract pollinators or determine pollen placement. While most species in
Centropogon (Campanulaceae: Lobelioideae) have flowers that suggest adaptation to bat or hummingbird pollination, actual pollinators are rarely documented, and a few species have a mix of traits from both pollination syndromes. We studied the pollination biology of a “mixed‐syndrome” species and its co‐occurring congeners to examine the relationship between floral traits and visitation patterns forCentropogon .Methods Fieldwork at two sites in Bolivian cloud forests involved filming floral visitors, quantifying pollen transfer, and measuring floral traits. Stamen exsertion, which determines pollen placement, was measured from herbarium specimens across the geographic range of these species to test for character displacement.
Results Results show a generalization gradient, from primarily bat pollination in white‐flowered
Centropogon incanus , to bat pollination with secondary hummingbird pollination in the cream‐floweredC. brittonianus , to equal reliance on both pollinators in the red‐flowered, mixed‐syndromeC. mandonis . Pollen transfer between these species is further reduced by differences in stamen exsertion that are accentuated in zones of sympatry, a pattern consistent with character displacement.Conclusions Our results demonstrate that key differences in floral color and shape mediate a gradient of specialization in Bolivian
Centropogon . Interspecific pollen transfer is further reduced by potential character displacement of a key trait. Broadly, our results have implications for understanding the hyper‐diversity of Andean cloud forests, in which multiple species of the same genus frequently co‐occur.
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fpls.2022.945806
