skip to main content


Title: Cycad-Weevil Pollination Symbiosis Is Characterized by Rapidly Evolving and Highly Specific Plant-Insect Chemical Communication
Coevolution between plants and insects is thought to be responsible for generating biodiversity. Extensive research has focused largely on antagonistic herbivorous relationships, but mutualistic pollination systems also likely contribute to diversification. Here we describe an example of chemically-mediated mutualistic species interactions affecting trait evolution and lineage diversification. We show that volatile compounds produced by closely related species of Zamia cycads are more strikingly different from each other than are other phenotypic characters, and that two distantly related pollinating weevil species have specialized responses only to volatiles from their specific host Zamia species. Plant transcriptomes show that approximately a fifth of genes related to volatile production are evolving under positive selection, but we find no differences in the relative proportion of genes under positive selection in different categories. The importance of phenotypic divergence coupled with chemical communication for the maintenance of this obligate mutualism highlights chemical signaling as a key mechanism of coevolution between cycads and their weevil pollinators.  more » « less
Award ID(s):
1906333
NSF-PAR ID:
10284928
Author(s) / Creator(s):
; ; ; ; ;
Date Published:
Journal Name:
Frontiers in Plant Science
Volume:
12
ISSN:
1664-462X
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Background and Aims

    Cycads are a key lineage to understand the early evolution of seed plants and their response to past environmental changes. However, tracing the evolutionary trajectory of cycad species is challenging when the robust relationships at inter- or infrageneric level are not well resolved.

    Methods

    Here, using 2901 single-copy nuclear genes, we explored the species relationships and gene flow within the second largest genus of cycads, i.e. Zamia, based on phylotranscriptomic analyses of 90 % extant Zamia species. Based on a well-resolved phylogenetic framework, we performed gene flow analyses, molecular dating and biogeographical reconstruction to examine the spatiotemporal evolution of Zamia. We also performed ancestral state reconstruction of a total of 62 traits of the genus to comprehensively investigate its morphological evolution.

    Key Results

    Zamia comprises seven major clades corresponding to seven distinct distribution areas in the Americas, with at least three reticulation nodes revealed in this genus. Extant lineages of Zamia initially diversified around 18.4–32.6 (29.14) million years ago in Mega-Mexico, and then expanded eastward into the Caribbean and southward into Central and South America. Ancestral state reconstruction revealed homoplasy in most of the morphological characters.

    Conclusions

    This study revealed congruent phylogenetic relationships from comparative methods/datasets, with some conflicts being the result of incomplete lineage sorting and ancient/recent hybridization events. The strong association between the clades and the biogeographic areas suggested that ancient dispersal events shaped the modern distribution pattern, and regional climatic factors may have resulted in the following in situ diversification. Climate cooling starting during the mid-Miocene is associated with the global expansion of Zamia to tropical South America that has dramatically driven lineage diversification in the New World flora, as well as the extinction of cycad species in the nowadays cooler regions of both hemispheres, as indicated by the fossil records.

     
    more » « less
  2. Alba, Mar (Ed.)
    Abstract Adaptive radiations are characterised by the diversification and ecological differentiation of species, and replicated cases of this process provide natural experiments for understanding the repeatability and pace of molecular evolution. During adaptive radiation, genes related to ecological specialisation may be subject to recurrent positive directional selection. However, it is not clear to what extent patterns of lineage-specific ecological specialisation (including phenotypic convergence) are correlated with shared signatures of molecular evolution. To test this, we sequenced whole exomes from a phylogenetically dispersed sample of 38 murine rodent species, a group characterised by multiple, nested adaptive radiations comprising extensive ecological and phenotypic diversity. We found that genes associated with immunity, reproduction, diet, digestion and taste have been subject to pervasive positive selection during the diversification of murine rodents. We also found a significant correlation between genome-wide positive selection and dietary specialisation, with a higher proportion of positively selected codon sites in derived dietary forms (i.e. carnivores and herbivores) than in ancestral forms (i.e. omnivores). Despite striking convergent evolution of skull morphology and dentition in two distantly related worm-eating specialists, we did not detect more genes with shared signatures of positive or relaxed selection than in a non-convergent species comparison. While a small number of the genes we detected can be incidentally linked to craniofacial morphology or diet, protein-coding regions are unlikely to be the primary genetic basis of this complex convergent phenotype. Our results suggest a link between positive selection and derived ecological phenotypes, and highlight specific genes and general functional categories that may have played an integral role in the extensive and rapid diversification of murine rodents. 
    more » « less
  3. Abstract

    Ecological interactions shape the evolution of multiple species traits in populations. These traits are often linked to each other through genetic correlations, affecting how each trait evolves through selection imposed by interacting partners. Here, we integrate quantitative genetics, coevolutionary theory and network science to explore how trait correlations affect the coevolution of mutualistic species not only in pairs of species but also in species‐rich networks across space. We show that genetic correlations may determine the pace of coevolutionary change, affect species abundances and fuel divergence among populations of the same species. However, this trait divergence promoted by genetic correlations is partially buffered by the nested structure of species‐rich mutualisms. Our study, therefore, highlights how coevolution and its ecological consequences may result from conflicting processes at different levels of organisation, ranging from genes to communities.

     
    more » « less
  4. ABSTRACT Plant pathogens utilize a portfolio of secreted effectors to successfully infect and manipulate their hosts. It is, however, still unclear whether changes in secretomes leading to host specialization involve mostly effector gene gains/losses or changes in their sequences. To test these hypotheses, we compared the secretomes of three host-specific castrating anther smut fungi ( Microbotryum ), two being sister species. To address within-species evolution, which might involve coevolution and local adaptation, we compared the secretomes of strains from differentiated populations. We experimentally validated a subset of signal peptides. Secretomes ranged from 321 to 445 predicted secreted proteins (SPs), including a few species-specific proteins (42 to 75), and limited copy number variation, i.e., little gene family expansion or reduction. Between 52% and 68% of the SPs did not match any Pfam domain, a percentage that reached 80% for the small secreted proteins, indicating rapid evolution. In comparison to background genes, we indeed found SPs to be more differentiated among species and strains, more often under positive selection, and highly expressed in planta ; repeat-induced point mutations (RIPs) had no role in effector diversification, as SPs were not closer to transposable elements than background genes and were not more RIP affected. Our study thus identified both conserved core proteins, likely required for the pathogenic life cycle of all Microbotryum species, and proteins that were species specific or evolving under positive selection; these proteins may be involved in host specialization and/or coevolution. Most changes among closely related host-specific pathogens, however, involved rapid changes in sequences rather than gene gains/losses. IMPORTANCE Plant pathogens use molecular weapons to successfully infect their hosts, secreting a large portfolio of various proteins and enzymes. Different plant species are often parasitized by host-specific pathogens; however, it is still unclear whether the molecular basis of such host specialization involves species-specific weapons or different variants of the same weapons. We therefore compared the genes encoding secreted proteins in three plant-castrating pathogens parasitizing different host plants, producing their spores in plant anthers by replacing pollen. We validated our predictions for secretion signals for some genes and checked that our predicted secreted proteins were often highly expressed during plant infection. While we found few species-specific secreted proteins, numerous genes encoding secreted proteins showed signs of rapid evolution and of natural selection. Our study thus found that most changes among closely related host-specific pathogens involved rapid adaptive changes in shared molecular weapons rather than innovations for new weapons. 
    more » « less
  5. Abstract Seminal fluid proteins (SFPs) mediate an array of postmating reproductive processes that influence fertilization and fertility. As such, it is widely held that SFPs may contribute to postmating, prezygotic reproductive barriers between closely related taxa. We investigated seminal fluid (SF) diversification in a recently diverged passerine species pair (Passer domesticus and Passer hispaniolensis) using a combination of proteomic and comparative evolutionary genomic approaches. First, we characterized and compared the SF proteome of the two species, revealing consistencies with known aspects of SFP biology and function in other taxa, including the presence and diversification of proteins involved in immunity and sperm maturation. Second, using whole-genome resequencing data, we assessed patterns of genomic differentiation between house and Spanish sparrows. These analyses detected divergent selection on immunity-related SF genes and positive selective sweeps in regions containing a number of SF genes that also exhibited protein abundance diversification between species. Finally, we analyzed the molecular evolution of SFPs across 11 passerine species and found a significantly higher rate of positive selection in SFPs compared with the rest of the genome, as well as significant enrichments for functional pathways related to immunity in the set of positively selected SF genes. Our results suggest that selection on immunity pathways is an important determinant of passerine SF composition and evolution. Assessing the role of immunity genes in speciation in other recently diverged taxa should be prioritized given the potential role for immunity-related proteins in reproductive incompatibilities in Passer sparrows. 
    more » « less