Title: Genome‐scale data resolves the timing of divergence in Joshua trees
Premise
Joshua trees (Yucca brevifoliaandY. jaegeriana) and their yucca moth pollinators (Tegeticula syntheticaandT. antithetica) are a model system for studies of plant–pollinator coevolution and, they are thought to be one of the only cases in which there is compelling evidence for cospeciation driven by coevolution. Previous work attempted to evaluate whether divergence between the plant and their pollinators was contemporaneous. That work concluded that the trees diverged more than 5 million years ago—well before the pollinators. However, clear inferences were hampered by a lack of data from the nuclear genome and low genetic variation in chloroplast genes. As a result, divergence times in the trees could not be confidently estimated.
Methods
We present an analysis of whole chloroplast genome sequence data and RADseq data from >5000 loci in the nuclear genome. We developed a molecular clock for the Asparagales and the Agavoideae using multiple fossil calibration points. Using Bayesian inference, we produced new estimates for the age of the genusYuccaand for Joshua trees. We used calculated summary statistics describing genetic variation and used coalescent‐based methods to estimate population genetic parameters.
Results
We find that the Joshua trees are moderately genetically differentiated, but that they diverged quite recently (~100–200 kya), and much more recently than their pollinators.
Conclusions
The results argue against the notion that coevolution directly contributed to speciation in this system, suggesting instead that coevolution with pollinators may have reinforced reproductive isolation following initial divergence in allopatry.
Spriggs, Elizabeth L.; Schlutius, Caroline; Eaton, Deren A.; Park, Brian; Sweeney, Patrick W.; Edwards, Erika J.; Donoghue, Michael J.(
, American Journal of Botany)
Premise
We take an integrative approach in assessing how introgression and Pleistocene climate fluctuations have shaped the diversification of the coreLentagoclade ofViburnum, a group of five interfertile species with broad areas of sympatry. We specifically tested whether flowering time plays a role in maintaining species isolation.
Methods
RAD‐seq data for 103 individuals were used to infer the species relationships and the genetic structure within each species. Flowering times were compared among species on the basis of historical flowering dates documented by herbarium specimens.
Results
Within each species, we found a strong relationship between flowering date and latitude, such that southern populations flower earlier than northern ones. In areas of sympatry, the species flower in sequence rather than simultaneously, with flowering dates offset by ≥9 d for all species pairs. In two cases it appears that the offset in flowering times is an incidental consequence of adaptation to differing climates, but in the recently diverged sister speciesV. prunifoliumandV. rufidulum, we find evidence that reinforcement led to reproductive character displacement. Long‐term trends suggest that the two northern‐most species are flowering earlier in response to recent climate change.
Conclusions
We argue that speciation in theLentagoclade has primarily occurred through ecological divergence of allopatric populations, but differences in flowering time were essential to maintain separation of incipient species when they came into secondary contact. This combination of factors may underlie diversification in many other plant clades.
Pellmyr, Olle; Kjellberg, Finn; Herre, Edward Allen; Kawakita, Atsushi; Hembry, David H.; Holland, J. Nathaniel; Terrazas, Teresa; Clement, Wendy; Segraves, Kari A.; Althoff, David M.(
, American Journal of Botany)
Premise
Variation in pollen‐ovule ratios is thought to reflect the degree of pollen transfer efficiency—the more efficient the process, the fewer pollen grains needed. Few studies have directly examined the relationship between pollen‐ovule ratio and pollen transfer efficiency. For active pollination in the pollination brood mutualisms of yuccas and yucca moths, figs and fig wasps, senita and senita moths, and leafflowers and leafflower moths, pollinators purposefully collect pollen and place it directly on the stigmatic surface of conspecific flowers. The tight coupling of insect reproductive interests with pollination of the flowers in which larvae develop ensures that pollination is highly efficient.
Methods
We used the multiple evolutionary transitions between passive pollination and more efficient active pollination to test if increased pollen transfer efficiency leads to reduced pollen‐ovule ratios. We collected pollen and ovule data from a suite of plant species from each of the pollination brood mutualisms and used phylogenetically controlled tests and sister‐group comparisons to examine whether the shift to active pollination resulted in reduced pollen‐ovule ratios.
Results
Across all transitions between passive and active pollination in plants, actively pollinated plants had significantly lower pollen‐ovule ratios than closely related passively pollinated taxa. Phylogenetically corrected comparisons demonstrated that actively pollinated plant species had an average 76% reduction in the pollen‐ovule ratio.
Conclusions
The results for active pollination systems support the general utility of pollen‐ovule ratios as indicators of pollination efficiency and the central importance of pollen transfer efficiency in the evolution of pollen‐ovule ratio.
Levin, Rachel A.; Miller, Jill S.(
, American Journal of Botany)
Premise
Long‐distance dispersal has been important in explaining the present distributions of many plant species. Despite being infrequent, such dispersal events have considerable evolutionary consequences, because bottlenecks during colonization can result in reduced genetic diversity. We examined the phylogeographic history ofLycium carolinianum, a widespread taxon that ranges from southeastern North America to several Pacific islands, with intraspecific diversity in sexual and mating systems.
Methods
We used Bayesian, likelihood, and coalescent approaches with nuclear and plastid sequence data and genome‐wide single nucleotide polymorphisms to reconstruct the dispersal history of this species. We also compared patterns of genetic variation in mainland and island populations using single nucleotide polymorphisms and allelic diversity at theS‐RNasemating system gene.
Results
Lycium carolinianumis monophyletic and dispersed once from the North American mainland, colonizing the Pacific islands ca. 40,100 years ago. This dispersal was accompanied by a loss of genetic diversity in SNPs and theS‐RNaselocus due to a colonization bottleneck and the loss of self‐incompatibility. Additionally, we documented at least two independent transitions to gynodioecy: once following the colonization of the Hawaiian Islands and loss of self‐incompatibility, and a second time associated with polyploidy in the Yucatán region of Mexico.
Conclusions
Long‐distance dispersal via fleshy, bird dispersed fruits best explains the unusually widespread distribution ofL. carolinianum. The collapse of diversity at theS‐RNaselocus in island populations suggests that self‐fertilization may have facilitated the subsequent colonization of Pacific islands following a single dispersal from mainland North America.
Straub, Shannon C. K.; Boutte, Julien; Fishbein, Mark; Livshultz, Tatyana(
, Applications in Plant Sciences)
Premise
Apocynaceae is the 10th largest flowering plant family and a focus for study of plant–insect interactions, especially as mediated by secondary metabolites. However, it has few genomic resources relative to its size. Target capture sequencing is a powerful approach for genome reduction that facilitates studies requiring data from the nuclear genome in non‐model taxa, such as Apocynaceae.
Methods
Transcriptomes were used to design probes for targeted sequencing of putatively single‐copy nuclear genes across Apocynaceae. The sequences obtained were used to assess the success of the probe design, the intrageneric and intraspecific variation in the targeted genes, and the utility of the genes for inferring phylogeny.
Results
From 853 candidate nuclear genes, 835 were consistently recovered in single copy and were variable enough for phylogenomics. The inferred gene trees were useful for coalescent‐based species tree analysis, which showed all subfamilies of Apocynaceae as monophyletic, while also resolving relationships among species within the genusApocynum. Intraspecific comparison ofElytropus chilensisindividuals revealed numerous single‐nucleotide polymorphisms with potential for use in population‐level studies.
Discussion
Community use of this Hyb‐Seq probe set will facilitate and promote progress in the study of Apocynaceae across scales from population genomics to phylogenomics.
Wenzell, Katherine E.; McDonnell, Angela J.; Wickett, Norman J.; Fant, Jeremie B.; Skogen, Krissa A.(
, American Journal of Botany)
Premise
Divergence depends on the strength of selection and frequency of gene flow between taxa, while reproductive isolation relies on mating barriers and geographic distance. Less is known about how these processes interact at early stages of speciation. Here, we compared population‐level differentiation in floral phenotype and genetic sequence variation among recently divergedCastillejato explore patterns of diversification under different scenarios of reproductive isolation.
Methods
Using target enrichment enabled by the Angiosperms353 probe set, we assessed genetic distance among 50 populations of fourCastillejaspecies. We investigated whether patterns of genetic divergence are explained by floral trait variation or geographic distance in two focal groups: the widespreadC. sessilifloraand the more restrictedC. purpureaspecies complex.
Results
We document thatC. sessilifloraand theC. purpureacomplex are characterized by high diversity in floral color across varying geographic scales. Despite phenotypic divergence, groups were not well supported in phylogenetic analyses, and little genetic differentiation was found across targeted Angiosperms353 loci. Nonetheless, a principal coordinate analysis of single nucleotide polymorphisms revealed differentiation withinC. sessilifloraacross floral morphs and geography and less differentiation among species of theC. purpureacomplex.
Conclusions
Patterns of genetic distance inC. sessiliflorasuggest species cohesion maintained over long distances despite variation in floral traits. In theC. purpureacomplex, divergence in floral color across narrow geographic clines may be driven by recent selection on floral color. These contrasting patterns of floral and genetic differentiation reveal that divergence can arise via multiple eco‐evolutionary paths.
Smith, Christopher Irwin, McKain, Michael R., Guimond, Austin, and Flatz, Ramona. Genome‐scale data resolves the timing of divergence in Joshua trees. American Journal of Botany 108.4 Web. doi:10.1002/ajb2.1633.
Smith, Christopher Irwin, McKain, Michael R., Guimond, Austin, & Flatz, Ramona. Genome‐scale data resolves the timing of divergence in Joshua trees. American Journal of Botany, 108 (4). https://doi.org/10.1002/ajb2.1633
Smith, Christopher Irwin, McKain, Michael R., Guimond, Austin, and Flatz, Ramona.
"Genome‐scale data resolves the timing of divergence in Joshua trees". American Journal of Botany 108 (4). Country unknown/Code not available: Wiley Blackwell (John Wiley & Sons). https://doi.org/10.1002/ajb2.1633.https://par.nsf.gov/biblio/10237042.
@article{osti_10237042,
place = {Country unknown/Code not available},
title = {Genome‐scale data resolves the timing of divergence in Joshua trees},
url = {https://par.nsf.gov/biblio/10237042},
DOI = {10.1002/ajb2.1633},
abstractNote = {PremiseJoshua trees (Yucca brevifoliaandY. jaegeriana) and their yucca moth pollinators (Tegeticula syntheticaandT. antithetica) are a model system for studies of plant–pollinator coevolution and, they are thought to be one of the only cases in which there is compelling evidence for cospeciation driven by coevolution. Previous work attempted to evaluate whether divergence between the plant and their pollinators was contemporaneous. That work concluded that the trees diverged more than 5 million years ago—well before the pollinators. However, clear inferences were hampered by a lack of data from the nuclear genome and low genetic variation in chloroplast genes. As a result, divergence times in the trees could not be confidently estimated. MethodsWe present an analysis of whole chloroplast genome sequence data and RADseq data from >5000 loci in the nuclear genome. We developed a molecular clock for the Asparagales and the Agavoideae using multiple fossil calibration points. Using Bayesian inference, we produced new estimates for the age of the genusYuccaand for Joshua trees. We used calculated summary statistics describing genetic variation and used coalescent‐based methods to estimate population genetic parameters. ResultsWe find that the Joshua trees are moderately genetically differentiated, but that they diverged quite recently (~100–200 kya), and much more recently than their pollinators. ConclusionsThe results argue against the notion that coevolution directly contributed to speciation in this system, suggesting instead that coevolution with pollinators may have reinforced reproductive isolation following initial divergence in allopatry.},
journal = {American Journal of Botany},
volume = {108},
number = {4},
publisher = {Wiley Blackwell (John Wiley & Sons)},
author = {Smith, Christopher Irwin and McKain, Michael R. and Guimond, Austin and Flatz, Ramona},
}
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