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
A striking characteristic of the Western North American flora is the repeated evolution of hummingbird pollination from insect-pollinated ancestors. This pattern has received extensive attention as an opportunity to study repeated trait evolution as well as potential constraints on evolutionary reversibility, with little attention focused on the impact of these transitions on species diversification rates. Yet traits conferring adaptation to divergent pollinators potentially impact speciation and extinction rates, because pollinators facilitate plant reproduction and specify mating patterns between flowering plants. Here, we examine macroevolutionary processes affecting floral pollination syndrome diversity in the largest North American genus of flowering plants, Penstemon. Within Penstemon, transitions from ancestral bee-adapted flowers to hummingbird-adapted flowers have frequently occurred, although hummingbird-adapted species are rare overall within the genus. We inferred macroevolutionary transition and state-dependent diversification rates and found that transitions from ancestral bee-adapted flowers to hummingbird-adapted flowers are associated with reduced net diversification rate, a finding based on an estimated 17 origins of hummingbird pollination in our sample. Although this finding is congruent with hypotheses that hummingbird adaptation in North American Flora is associated with reduced species diversification rates, it contrasts with studies of neotropical plant families where hummingbird pollination has been associated with increased species diversification. We further used the estimated macroevolutionary rates to predict the expected pattern of floral diversity within Penstemon over time, assuming stable diversification and transition rates. Under these assumptions, we find that hummingbird-adapted species are expected to remain rare due to their reduced diversification rates. In fact, current floral diversity in the sampled Penstemon lineage, where less than one-fifth of species are hummingbird adapted, is consistent with predicted levels of diversity under stable macroevolutionary rates.
more » « less- NSF-PAR ID:
- 10384205
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Evolution Letters
- Volume:
- 3
- Issue:
- 5
- ISSN:
- 2056-3744
- Page Range / eLocation ID:
- p. 521-533
- 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 Premise A switch in pollinator can occur when a plant lineage enters a new habitat where the ancestral pollinator is less common, and a novel pollinator is more common. Because pollinator communities vary according to environmental tolerances and availability of resources, there may be consistent associations between pollination mode and specific regions and habitats. Such associations can be studied in lineages that have experienced multiple pollinator transitions, representing evolutionary replicates.
Methods Our study focused on a large clade of
Penstemon wildflower species in western North America, which has repeatedly evolved hummingbird‐adapted flowers from ancestral bee‐adapted flowers. For each species, we estimated geographic ranges from occurrence data and inferred environmental niches from climate, topographical, and soil data. Using a phylogenetic comparative approach, we investigated whether hummingbird‐adapted species occupy distinct geographic regions or habitats relative to bee‐adapted species.Results Hummingbird‐adapted species occur at lower latitudes and lower elevations than bee‐adapted species, resulting in a difference in their environmental niche. Bee‐adapted species sister to hummingbird‐adapted species are also found in relatively low elevations and latitudes, similar to their hummingbird‐adapted sister species, suggesting ecogeographic shifts precede pollinator divergence. Sister species pairs—regardless of whether they differ in pollinator—show relatively little geographic range overlap.
Conclusions Adaptation to a novel pollinator may often occur in geographic and ecological isolation from ancestral populations. The ability of a given lineage to adapt to novel pollinators may critically depend on its ability to colonize regions and habitats associated with novel pollinator communities.
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Premise: A switch in pollinator can occur when a plant lineage enters a new habitat where the ancestral pollinator is less common and a novel pollinator is more common. Since pollinator communities vary according to environmental tolerances and availability of resources, there may be consistent associations between pollination mode and specific regions and habitats. Such associations can be studied in lineages that have experienced multiple pollinator transitions, representing evolutionary replicates. Methods: Our study focused on a large clade of Penstemon wildflower species in western North America that has repeatedly evolved hummingbird-adapted flowers from ancestral bee-adapted flowers. For each species, we estimated geographic ranges from occurrence data and inferred environmental niches from climate, topographical, and soil data. Using a phylogenetic comparative approach, we investigated whether hummingbird-adapted species occupy distinct geographic regions or habitats relative to beeadapted species. Results: Hummingbird-adapted species occur at lower latitudes and lower elevations than bee-adapted species, resulting in a difference in their environmental niche. Hummingbird-adapted species seem to evolve in lineages that previously adapted to lower latitudes and elevations, since bee-adapted species sister to hummingbird-adapted species also occur in these regions and habitats. Sister species pairs – regardless of whether they differ in pollinator – show relatively little geographic range overlap. Conclusions: Adaptation to a novel pollinator may often occur in geographic and ecological isolation from ancestral populations. The ability of a given lineage to adapt to novel pollinators may critically depend on its ability to colonize regions and habitats associated with novel pollinator communities.more » « less
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Summary Evolution of complex phenotypes depends on the adaptive importance of individual traits, and the developmental changes required to modify traits. Floral syndromes are complex adaptations to pollinators that include color, nectar, and shape variation. Hummingbird‐adapted flowers have evolved a remarkable number of times from bee‐adapted ancestors in
Penstemon , and previous work demonstrates that color over shape better distinguishes bee from hummingbird syndromes. Here, we examined the relative importance of nectar volume and nectary development in definingPenstemon pollination syndromes.We tested the evolutionary association of nectar volume and nectary area with pollination syndrome across 19
Penstemon species. In selected species, we assessed cellular‐level processes shaping nectary size. Within a segregating population from an intersyndrome cross, we assessed trait correlations between nectar volume, nectary area, and the size of stamens on which nectaries develop.Nectar volume and nectary area displayed an evolutionary association with pollination syndrome. These traits were correlated within a genetic cross, suggesting a mechanistic link. Nectary area evolution involves parallel processes of cell expansion and proliferation.
Our results demonstrate that changes to nectary patterning are an important contributor to pollination syndrome diversity and provide further evidence that repeated origins of hummingbird adaptation involve parallel developmental processes in
Penstemon .
