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Adaptation to hummingbird pollination is associated with reduced diversification in Penstemon.

ABSTRACT: 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.

SUBMITTER: Wessinger CA

PROVIDER: S-EPMC6791294 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Adaptation to hummingbird pollination is associated with reduced diversification in <i>Penstemon</i>.

Wessinger Carolyn A CA Rausher Mark D MD Hileman Lena C LC

Evolution letters 20190802 5

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 an ...[more]

PMID: 31636944

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Project description:Distinct floral pollination syndromes have emerged multiple times during the diversification of flowering plants. For example, in western North America, a hummingbird pollination syndrome has evolved more than 100 times, generally from within insect-pollinated lineages. The hummingbird syndrome is characterized by a suite of floral traits that attracts and facilitates pollen movement by hummingbirds, while at the same time discourages bee visitation. These floral traits generally include large nectar volume, red flower colour, elongated and narrow corolla tubes and reproductive organs that are exerted from the corolla. A handful of studies have examined the genetic architecture of hummingbird pollination syndrome evolution. These studies find that mutations of relatively large effect often explain increased nectar volume and transition to red flower colour. In addition, they suggest that adaptive suites of floral traits may often exhibit a high degree of genetic linkage, which could facilitate their fixation during pollination syndrome evolution. Here, we explore these emerging generalities by investigating the genetic basis of floral pollination syndrome divergence between two related Penstemon species with different pollination syndromes--bee-pollinated P. neomexicanus and closely related hummingbird-pollinated P. barbatus. In an F2 mapping population derived from a cross between these two species, we characterized the effect size of genetic loci underlying floral trait divergence associated with the transition to bird pollination, as well as correlation structure of floral trait variation. We find the effect sizes of quantitative trait loci for adaptive floral traits are in line with patterns observed in previous studies, and find strong evidence that suites of floral traits are genetically linked. This linkage may be due to genetic proximity or pleiotropic effects of single causative loci. Interestingly, our data suggest that the evolution of floral traits critical for hummingbird pollination was not constrained by negative pleiotropy at loci that show co-localization for multiple traits.

Project description:In many plant species, pollination syndromes predict the most effective pollinator. However, other floral visitors may also offer effective pollination services and promote mixed pollination systems. Several species of the species-rich Penstemon (Plantaginaceae) exhibit a suite of floral traits that suggest adaptation for pollination by both hymenopterans and hummingbirds. Transitions from the ancestral hymenopteran pollination syndrome to more derived hummingbird pollination syndrome may be promoted if the quantity or quality of visits by hummingbirds is increased and if the ancestral pollinator group performs less efficiently. The quantification of such shifts in pollination systems in the group is still limited. We aimed to investigate floral traits linked to this pollination syndrome in Penstemon gentianoides with flowers visited by bumblebees and hummingbirds.We investigated the floral biology, pollinator assemblages, breeding system and nectar production patterns of P. gentianoides inhabiting a temperate montane forest in central Mexico. Pollination experiments were also conducted to assess the pollinator effectiveness of bumblebees and hummingbirds.P. gentianoides flowers are protandrous, with 8-d male phase (staminate) flowers, followed by the ∼1-7 d female phase (pistillate phase). Flowers display traits associated with hymenopteran pollination, including purple flowers abruptly ampliate-ventricose to a broad throat with anthers and stigmas included, and long lifespans. However, the nectar available in the morning hours was abundant and dilute, traits linked to flowers with a hummingbird pollination syndrome. Two hummingbird species made most of the visits to flowers, Selasphorus platycercus (30.3% of all visits), followed by Archilochus colubris (11.3%). Bumblebees (Bombus ephippiatus, B. huntii and B. weisi) accounted for 51.8% of all recorded visits, but their foraging activity was restricted to the warmer hours. Hummingbirds made more foraging bouts and visited more flowers than hymenopteran species. Flowers experimentally pollinated by B. ephippiatus produced significantly more fruits than those pollinated by S. platycercus. However, there was no statistical difference in the number of seeds produced per fruit when a bumblebee or a hummingbird was the pollinator.We have shown that bumblebees and hummingbirds visit and pollinate P. gentianoides flowers. Despite floral traits resembling the hymenoptera pollination syndrome, flowers of P. gentianoides offer characteristic nectar rewards to flowers with a hummingbird pollination syndrome. Although pollination efficiency is higher among flowers visited by hymenoptera, the noteworthy percentage of fruit production and number of seeds per fruit derived from hummingbird pollination highlights the importance of hummingbirds as a functional group of pollinators that might have potential evolutionary consequences to the plants.

Dataset Information

Adaptation to hummingbird pollination is associated with reduced diversification in Penstemon.

Publications

Adaptation to hummingbird pollination is associated with reduced diversification in <i>Penstemon</i>.

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