hummingbird pollination
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EvoDevo ◽  
2022 ◽  
Vol 13 (1) ◽  
Author(s):  
Marina M. Strelin ◽  
Eduardo E. Zattara ◽  
Kristian Ullrich ◽  
Mareike Schallenberg-Rüdinger ◽  
Stefan Rensing

Abstract Background Understanding the relationship between macroevolutionary diversity and variation in organism development is an important goal of evolutionary biology. Variation in the morphology of several plant and animal lineages is attributed to pedomorphosis, a case of heterochrony, where an ancestral juvenile shape is retained in an adult descendant. Pedomorphosis facilitated morphological adaptation in different plant lineages, but its cellular and molecular basis needs further exploration. Plant development differs from animal development in that cells are enclosed by cell walls and do not migrate. Moreover, in many plant lineages, the differentiated epidermis of leaves, and leaf-derived structures, such as petals, limits organ growth. We, therefore, proposed that pedomorphosis in leaves, and in leaf-derived structures, results from delayed differentiation of epidermal cells with respect to reproductive maturity. This idea was explored for petal evolution, given the importance of corolla morphology for angiosperm reproductive success. Results By comparing cell morphology and transcriptional profiles between 5 mm flower buds and mature flowers of an entomophile and an ornitophile Loasoideae species (a lineage that experienced transitions from bee- to hummingbird-pollination), we show that evolution of pedomorphic petals of the ornithophile species likely involved delayed differentiation of epidermal cells with respect to flower maturity. We also found that developmental mechanisms other than pedomorphosis might have contributed to evolution of corolla morphology. Conclusions Our results highlight a need for considering alternatives to the flower-centric perspective when studying the origin of variation in flower morphology, as this can be generated by developmental processes that are also shared with leaves. Graphical Abstract


2021 ◽  
Author(s):  
Molly B. Edwards ◽  
Gary P. T. Choi ◽  
Nathan J. Derieg ◽  
Ya Min ◽  
Angie C. Diana ◽  
...  

Interactions with animal pollinators have helped shape the stunning diversity of flower morphologies across the angiosperms. A common evolutionary consequence of these interactions is that some flowers have converged on suites of traits, or pollination syndromes, that attract and reward specific pollinator groups. Determining the genetic basis of these floral pollination syndromes can help us understand the processes that contributed to the diversification of the angiosperms. Here, we characterize the genetic architecture of a bee-to-hummingbird pollination shift in Aquilegia (columbine) using QTL mapping of 17 floral traits encompassing color, nectar composition, and organ morphology. In this system, we find that the genetic architectures underlying differences in floral color are quite complex, and we identify several likely candidate genes involved in anthocyanin and carotenoid floral pigmentation. Most morphological and nectar traits also have complex genetic underpinnings; however, one of the key floral morphological phenotypes, nectar spur curvature, is shaped by a single locus of large effect.


PLoS Genetics ◽  
2021 ◽  
Vol 17 (2) ◽  
pp. e1009095
Author(s):  
Thomas C. Nelson ◽  
Angela M. Stathos ◽  
Daniel D. Vanderpool ◽  
Findley R. Finseth ◽  
Yao-wu Yuan ◽  
...  

Inferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species). Taxa within Erythranthe, particularly the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M. cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M. lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele-sharing (Patterson’s D-statistic and related tests) indicate that gene-tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination and adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M. lewisii and M. cardinalis. Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M. lewisii and Southern Californian M. parishii each carrying organelle genomes nested within respective sympatric M. cardinalis clades. A recent organellar transfer from M. cardinalis, an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M. parishii organelles in hybrids with M. lewisii. Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation.


2021 ◽  
Author(s):  
Camila N Barrionuevo ◽  
Santiago Benitez-Vieyra ◽  
Federico Sazatornil

Abstract Aims Adaptive convergence in floral phenotype among plants sharing a pollinator guild has been acknowledged in the concept of pollination syndrome. However, many plants display traits associated with a given syndrome, but are visited by multiple pollinators. This situation may indicate the beginning of a pollinator shift or may result in a stable situation with adaptations to different pollinators. In Salvia stachydifolia, a previous study suggested that flower shape is optimized to maximize the contribution to pollination of bees and hummingbirds. Here, we studied three additional aspects of its floral biology: sexual phases, nectar dynamics and breeding system, and examined their connection with pollinators’ behavior to explore the presence of adaptations to bee and/or hummingbird pollination. Methods Using a greenhouse population, we applied five pollination treatments to characterize breeding system. To determine sexual phases, we recorded flower opening, anther dehiscence, corolla fall and stigma receptivity. Additionally, we characterized nectar volume and concentration dynamics along the day. Finally, to determine pollinator assemblage and visitation patterns, we performed field observations and recorded pollinators’ behavior. Important findings Salvia stachydifolia was partially protandrous and self-compatible, but open-pollinated plants attained the highest reproductive success, suggesting that reproduction is mainly dependent on pollinator activity. Bombus opifex bumblebees were the most frequent visitors, but Sappho sparganura hummingbirds dominated visits early in the morning and at dusk. Nectar was typical of bumblebee-pollination. We suggest that the bee-hummingbird mixed visitation constitutes an unstable evolutionary situation, making S. stachydifolia an ideal system to understand the ecological circumstances in which pollination shifts occur.


2020 ◽  
Vol 11 ◽  
Author(s):  
Ezgi Ogutcen ◽  
Karine Durand ◽  
Marina Wolowski ◽  
Laura Clavijo ◽  
Catherine Graham ◽  
...  

Changes in floral pigmentation can have dramatic effects on angiosperm evolution by making flowers either attractive or inconspicuous to different pollinator groups. Flower color largely depends on the type and abundance of pigments produced in the petals, but it is still unclear whether similar color signals rely on same biosynthetic pathways and to which extent the activation of certain pathways influences the course of floral color evolution. To address these questions, we investigated the physical and chemical aspects of floral color in the Neotropical Gesnerioideae (ca. 1,200 spp.), in which two types of anthocyanins, hydroxyanthocyanins, and deoxyanthocyanins, have been recorded as floral pigments. Using spectrophotometry, we measured flower reflectance for over 150 species representing different clades and pollination syndromes. We analyzed these reflectance data to estimate how the Gesnerioideae flowers are perceived by bees and hummingbirds using the visual system models of these pollinators. Floral anthocyanins were further identified using high performance liquid chromatography coupled to mass spectrometry. We found that orange/red floral colors in Gesnerioideae are produced either by deoxyanthocyanins (e.g., apigenidin, luteolinidin) or hydroxyanthocyanins (e.g., pelargonidin). The presence of deoxyanthocyanins in several lineages suggests that the activation of the deoxyanthocyanin pathway has evolved multiple times in the Gesnerioideae. The hydroxyanthocyanin-producing flowers span a wide range of colors, which enables them to be discriminated by hummingbirds or bees. By contrast, color diversity among the deoxyanthocyanin-producing species is lower and mainly represented at longer wavelengths, which is in line with the hue discrimination optima for hummingbirds. These results indicate that Gesnerioideae have evolved two different biochemical mechanisms to generate orange/red flowers, which is associated with hummingbird pollination. Our findings also suggest that the activation of the deoxyanthocyanin pathway has restricted flower color diversification to orange/red hues, supporting the potential constraining role of this alternative biosynthetic pathway on the evolutionary outcome of phenotypical and ecological diversification.


Author(s):  
Thomas C. Nelson ◽  
Angela M. Stathos ◽  
Daniel D. Vanderpool ◽  
Findley R. Finseth ◽  
Yao-wu Yuan ◽  
...  

AbstractInferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species). Taxa within Erythranthe, particularly the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M. cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M. lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele-sharing (Patterson’s D-statistic and related tests) indicate that gene-tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination and adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M. lewisii and M. cardinalis. Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M. lewisii and Southern Californian M. parishii each carrying organelle genomes nested within respective sympatric M. cardinalis clades. A recent organellar transfer from M. cardinalis, an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M. parishii organelles in hybrids with M. lewisii. Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation.Author SummaryAdaptive radiations, which involve both divergent evolution of new traits and recurrent trait evolution, provide insight into the processes that generate and maintain organismal diversity. However, rapid radiations also generate particular challenges for inferring the evolutionary history and mechanistic basis of adaptation and speciation, as multiple processes can cause different parts of the genome to have distinct phylogenetic trees. Thus, inferences about the mode and timing of divergence and the causes of parallel trait evolution require a fine-grained understanding of the flow of genomic variation through time. In this study, we used genome-wide sampling of thousands of genes to re-construct the evolutionary histories of a model plant radiation, the monkeyflowers of Mimulus section Erythranthe. Work over the past half-century has established the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated, as are three other species in the section) as textbook examples of both rapid speciation via shifts in pollination syndrome and convergent evolution of floral syndromes. Our phylogenomic analyses re-write both of these stories, placing M. cardinalis in a clade with other hummingbird-pollinated taxa and demonstrating that abundant introgression between ancestral lineages as well as in areas of current sympatry contributes to the real (but misleading) affinities between M. cardinalis and M. lewisii. This work illustrates the pervasive influence of gene flow and introgression during adaptive radiation and speciation, and underlines the necessity of a gene-scale and genome-wide phylogenomics framework for understanding trait divergence, even among well-established species.


2020 ◽  
Author(s):  
Benno I. Simmons ◽  
Andrew P. Beckerman ◽  
Katrine Hansen ◽  
Pietro K. Maruyama ◽  
Constantinos Televantos ◽  
...  

AbstractIndirect interactions are central to ecological and evolutionary dynamics in pollination communities, yet we have little understanding about the processes determining patterns of indirect interactions, such as those between pollinators through shared flowering plants. Instead, research has concentrated on the processes responsible for direct interactions and whole-network structures. This is partly due to a lack of appropriate tools for characterising indirect interaction structures, because traditional network metrics discard much of this information. The recent development of tools for counting motifs (subnetworks depicting interactions between a small number of species) in bipartite networks enable detailed analysis of indirect interaction patterns. Here we generate plant-hummingbird pollination networks based on three major assembly processes – neutral effects (species interacting in proportion to abundance), morphological matching and phenological overlap – and evaluate the motifs associated with each one. We find that different processes produce networks with significantly different patterns of indirect interactions. Neutral effects tend to produce densely-connected motifs, with short indirect interaction chains, and motifs where many specialists interact indirectly through a single generalist. Conversely, niche-based processes (morphology and phenology) produced motifs with a core of interacting generalists, supported by peripheral specialists. These results have important implications for understanding the processes determining indirect interaction structures.


PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e8778 ◽  
Author(s):  
Wade R. Roberts ◽  
Eric H. Roalson

Background Genetic pathways involved with flower color and shape are thought to play an important role in the development of flowers associated with different pollination syndromes, such as those associated with bee, butterfly, or hummingbird pollination. Because pollination syndromes are complex traits that are orchestrated by multiple genes and pathways, the gene regulatory networks have not been explored. Gene co-expression networks provide a systems level approach to identify important contributors to floral diversification. Methods RNA-sequencing was used to assay gene expression across two stages of flower development (an early bud and an intermediate stage) in 10 species of Achimenes (Gesneriaceae). Two stage-specific co-expression networks were created from 9,503 orthologs and analyzed to identify module hubs and the network periphery. Module association with bee, butterfly, and hummingbird pollination syndromes was tested using phylogenetic mixed models. The relationship between network connectivity and evolutionary rates (dN/dS) was tested using linear models. Results Networks contained 65 and 62 modules that were largely preserved between developmental stages and contained few stage-specific modules. Over a third of the modules in both networks were associated with flower color, shape, and pollination syndrome. Within these modules, several hub nodes were identified that related to the production of anthocyanin and carotenoid pigments and the development of flower shape. Evolutionary rates were decreased in highly connected genes and elevated in peripheral genes. Discussion This study aids in the understanding of the genetic architecture and network properties underlying the development of floral form and provides valuable candidate modules and genes for future studies.


Author(s):  
Leccinum Jesús García Morales ◽  
Rodrigo Homero González González ◽  
Jesús García Jiménez ◽  
Duilio Iamonico

Background and Aims: Cochemiea is a genus which currently comprises five species occurring in Mexico. It is morphologically characterized by cylindrical decumbent to prostrate stems and by a long red-scarlet zygomorphic perianth, presumably specialized for hummingbird pollination. As part ofthe ongoing taxonomic studies on the North Mexican flora, a population discovered by Thomas Linzen in 2012 in central Sinaloa (Mexico), previously identified as Mammillaria sp., actually refers to a Cochemiea species and cannot be ascribed to any of the known species of that genus. As a consequence,we here propose to describe this population as a a new species for science.Methods: The work is based on field surveys (autumn 2018 and spring 2019) in central Sinaloa, examination of herbarium specimens, and analysis of relevant literature. Its conservation status was assessed following the guidelines of the IUCN; AOO and EOO were calculated with the programGeoCAT.Key results: Cochemiea thomasii is described and illustrated from Sinaloa. The new species is morphologically similar to C. halei from which it differs by the hanging stems, the larger conical tubercles, less numerous and shorter central spines, and the ovoid fruits. A diagnostic key of the knownCochemiea species is included.Conclusions: Cochemiea thomasii is endemic to the state of Sinaloa where it occupies a small area. On the basis of the criteria B2a (geographic range) and C (small population) of IUCN, the new species can be assessed as Critically Endangered (CR) or Vulnerable (VU). Adopting the precautionary approach, Cochemiea thomasii is considered as Critically Endangered (CR).


2019 ◽  
Vol 192 (4) ◽  
pp. 592-608 ◽  
Author(s):  
Michael Kessler ◽  
Stefan Abrahamczyk ◽  
Thorsten Krömer

Abstract At least half of the 3600 species of Bromeliaceae are pollinated by hummingbirds. There is little doubt that the four to 12 evolutionary shifts towards and c. 32 shifts away from hummingbird pollination opened new evolutionary spaces for bromeliad diversification, and that hummingbird pollination has led to increased bromeliad diversification rates. However, the mechanisms leading to these increased rates remain unclear. We here propose that there are four main types of mechanisms that may increase diversification rates of hummingbird-pollinated bromeliad clades: (1) bromeliad speciation through adaptation to different hummingbird species; (2) increased allopatric speciation in hummingbird-pollinated clades due to lower pollen transfer efficiency compared with other pollinators; (3) differential speciation rates in hummingbird-pollinated clades dependent on of flowering phenology and hummingbird behaviour; and (4) higher speciation rates of bromeliads in montane environments (where hummingbird pollination predominates) due to topographic population fragmentation. To date, none of these hypotheses has been appropriately tested, partly due to a lack of data, but also because research so far has focused on documenting the pattern of increased diversification in hummingbird-pollinated clades, implicitly assuming that this pattern supports an underlying mechanism while ignoring the fact that several competing mechanisms may be considered. The aim of the present review is to increase awareness of these mechanisms and to trigger research aimed at specifically testing them. We conclude that much additional research on the roles of hummingbird behaviour and gene flow between bromeliad species is needed to elucidate their contribution to the evolution of diversity in bromeliads and other plant families.


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