skip to main content


Title: Polyploidy in creosote bush ( Larrea tridentata ) shapes the biogeography of specialist herbivores
Abstract Aim

Whole‐genome duplication (polyploidy) can influence the biogeography and ecology of plants that differ in ploidy level (cytotype). Here, we address how two consequences of plant polyploidy (parapatry of cytotypes and altered species interactions) shape the biogeography of herbivorous insects.

Location

Warm deserts of North America.

Taxa

Gall midges (Asphondylia auripilagroup, Diptera: Cecidomyiidae) that attack three parapatric cytotypes of creosote bush (Larrea tridentata, Zygophyllaceae).

Methods

We surveyedAsphondyliaspecies diversity at 177 sites across a 2300‐km extent. After noting a correspondence between the distributions of eightAsphondyliaspecies andL. tridentatacytotypes, we fine‐mappedAsphondyliaspecies range limits with transects spanning cytotype contact zones. We then tested whether plant–insect interactions and/or abiotic factors explain this coincidence by (a) comparing attack rates and gall midge communities on alternative cytotypes in a narrow zone of sympatry and (b) using species distribution models (SDMs) to determine if climatically suitable habitat for each midge species extended beyond cytotype contact zones.

Results

The range limits of 6/17Asphondyliaspecies (including two novel putative species confirmed withCOIsequencing) perfectly coincided with the contact zone of diploid and tetraploidL. tridentata. One midge species was restricted to diploid host plants while five were restricted to tetraploid and hexaploid host plants. Where diploid and tetraploidL. tridentataare sympatric, cytotype‐restricted midge species more frequently attacked their typical host andAsphondyliacommunity structure differed markedly between cytotypes.SDMs predicted that distributions of cytotype‐restricted midge species were not constrained by climatic conditions near cytotype contact zones.

Main conclusions

Contact zones between plant cytotypes are dispersal barriers for manyAsphondyliaspecies due to plant–insect interactions. The distribution ofL. tridentatacytotypes therefore shapes herbivore species ranges and herbivore community structure across North American deserts. Our results demonstrate that polyploidy in plants can affect the biogeography of ecological communities.

 
more » « less
NSF-PAR ID:
10084110
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Journal of Biogeography
Volume:
46
Issue:
3
ISSN:
0305-0270
Page Range / eLocation ID:
p. 597-610
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Premise

    Whole‐genome duplication (polyploidy) is an important force shaping flowering‐plant evolution. Ploidy‐specific plant–pollinator interactions represent important community‐level biotic interactions that can lead to nonrandom mating and the persistence of mixed‐ploidy populations.

    Methods

    At a naturally occurring diploid–tetraploid contact zone of the autopolyploid desert shrubLarrea tridentata, we combined flower phenology analyses, collections of bees on plants of known cytotype, and flow cytometry analyses of bee‐collected pollen loads to investigate whether (1) diploid and tetraploid plants have unique bee pollinator assemblages, (2) bee taxa exhibit ploidy‐specific visitation and pollen collection biases, and (3) specialist and generalist bee taxa have ploidy‐specific visitation and pollen collection biases.

    Results

    Although bee assemblages overlapped, we found significant differences in bee visitation to co‐occurring diploids and tetraploids, with the introduced honeybee (Apis mellifera) and one native species (Andrenaspecies 12) more frequently visiting tetraploids. Consistent with bee assemblage differences, we found that diploid pollen was overrepresented among pollen loads on native bees, while pollen loads onA. melliferadid not deviate from the random expectation. However, mismatches between the ploidy of pollen loads and plants were common, consistent with ongoing intercytotype gene flow.

    Conclusions

    Our data are consistent with cytotype‐specific bee visitation and suggest that pollinator behavior contributes to reduced diploid–tetraploid mating. Differences in bee visitation and pollen movement potentially contribute to an easing of minority cytotype exclusion and the facilitation of cytotype co‐occurrence.

     
    more » « less
  2. Abstract

    Host plant shifts are central to diversification in insect herbivores. Many mechanisms can cause host shifts in insects, but one relatively unexplored mechanism is whole‐genome duplication (WGD) in the host plant. WGD, or polyploidy, is common in plants and causes spontaneous changes in physiology, morphology, and palatability that could impact the ability of herbivores to feed and develop on newly formed polyploids (neopolyploids).

    Here the authors tested if WGD affected the preference and performance of the specialist aphid,Acyrthosiphon pisum(pea aphids). Pea aphids seasonally form specialised lineages or ‘host forms’ on many host plant species including alfalfa and red clover. Aphid host forms on alfalfa and red clover naturally exist on different cytotypes of their respective hosts, with red clover aphids feeding on diploid clover and alfalfa aphids feeding on tetraploid alfalfa. Therefore, the authors predicted that these host forms would have a higher preference for and performance on their respective natal host cytotype.

    Neither host form exhibited a preference for a particular cytotype, but there were modest changes in aphid performance based on host cytotype. Specifically, aphids specialised to red clover had higher fecundity on diploid red clover than on neotetraploid red clover. Together, these results showed that both host forms were able to recognise and accept different cytotypes of the two host species, but only one host form experienced trade‐offs in performance when feeding on neotetraploids. These results suggest that WGD may act as a mechanism of host expansion in pea aphids as plants speciate via WGD.

     
    more » « less
  3. Premise

    Although autopolyploidy is common among dominant Great Plains grasses, the distribution of cytotypes within a given species is typically poorly understood. This study aims to establish the geographic distribution of cytotypes within buffalograss (Buchloë dactyloides) and to assess whether individual cytotypes have differing ecological tolerances.

    Methods

    A range‐wide set of 578B. dactyloidesindividuals was obtained through field collecting and sampling from herbarium specimens. The cytotype of each sample was estimated by determining allele numbers at 13 simple sequence repeat loci, a strategy that was assessed by comparing estimated to known cytotype in 79 chromosome‐counted samples. Ecological differentiation between the dominant tetraploid and hexaploid cytotypes was assessed with analyses of macroclimatic variables.

    Results

    Simple sequence repeat variation accurately estimated cytotype in 89% of samples from which a chromosome count had been obtained. Applying this approach to samples of unknown ploidy established that diploids and pentaploids are rare, with the common tetraploid and hexaploid cytotypes generally occurring in sites to the north/west (tetraploid) or south/east (hexaploid) portions of the species range. BothMANOVAand niche modeling approaches identified significant but subtle differences in macroclimatic conditions at the set of locations occupied by these two dominant cytotypes.

    Conclusions

    Incorporating chromosome count vouchers and cytotype‐estimated herbarium records allowed us to perform the largest study of cytotype niche differentiation to date. Buffalograss cytotypes differ greatly in frequency, the common tetraploid and hexaploid cytotypes are non‐randomly distributed, and these two cytotypes are subtly ecologically differentiated.

     
    more » « less
  4. Premise

    Male gametophytes of most seed plants deliver sperm to eggs via a pollen tube. Pollen tube growth rates (PTGRs) of angiosperms are exceptionally rapid, a pattern attributed to more effective haploid selection under stronger pollen competition. Paradoxically, whole genome duplication (WGD) has been common in angiosperms but rare in gymnosperms. Pollen tube polyploidy should initially acceleratePTGRbecause increased heterozygosity and gene dosage should increase metabolic rates. However, polyploidy should also independently increase tube cell size, causing more work which should decelerate growth. We asked how genome size changes have affected the evolution of seed plantPTGRs.

    Methods

    We assembled a phylogenetic tree of 451 species with knownPTGRs. We then used comparative phylogenetic methods to detect effects of neo‐polyploidy (within‐genus origins),DNAcontent, andWGDhistory onPTGR, and correlated evolution ofPTGRandDNAcontent.

    Results

    Gymnosperms had significantly higherDNAcontent and slowerPTGRoptima than angiosperms, and theirPTGRandDNAcontent were negatively correlated. For angiosperms, 89% of model weight favored Ornstein‐Uhlenbeck models with a fasterPTGRoptimum for neo‐polyploids, whereasPTGRandDNAcontent were not correlated. For within‐genus and intraspecific‐cytotype pairs,PTGRs of neo‐polyploids < paleo‐polyploids.

    Conclusions

    Genome size increases should negatively affectPTGRwhen genetic consequences ofWGDs are minimized, as found in intra‐specific autopolyploids (low heterosis) and gymnosperms (fewWGDs). But in angiosperms, the higherPTGRoptimum of neo‐polyploids and non‐negativePTGRDNAcontent correlation suggest that recurrentWGDs have caused substantialPTGRevolution in a non‐haploid state.

     
    more » « less
  5. Current and past climatic changes can shift plant climatic niches, which may cause spatial overlap or separation between related taxa. The former often leads to hybridization and introgression, which may generate novel variation and influence the adaptive capacity of plants. An additional mechanism facilitating adaptations to novel environments and an important evolutionary driver in plants is polyploidy as the result of whole genome duplication. Artemisia tridentata (big sagebrush) is a landscape-dominating foundational shrub in the western United States which occupies distinct ecological niches, exhibiting diploid and tetraploid cytotypes. Tetraploids have a large impact on the species’ landscape dominance as they occupy a preponderance of the arid spectrum of A. tridentata range. Three distinct subspecies are recognized, which co-occur in ecotones – the transition zone between two or more distinct ecological niches – allowing for hybridization and introgression. Here we assess the genomic distinctiveness and extent of hybridization among subspecies at different ploidies under both contemporary and predicted future climates. We sampled five transects throughout the western United States where a subspecies overlap was predicted using subspecies-specific climate niche models. Along each transect, we sampled multiple plots representing the parental and the potential hybrid habitats. We performed reduced representation sequencing and processed the data using a ploidy-informed genotyping approach. Population genomic analyses revealed distinct diploid subspecies and at least two distinct tetraploid gene pools, indicating independent origins of the tetraploid populations. We detected low levels of hybridization (2.5%) between the diploid subspecies, while we found evidence for increased admixture between ploidy levels (18%), indicating hybridization has an important role in the formation of tetraploids. Our analyses highlight the importance of subspecies co-occurrence within these ecotones to maintain gene exchange and potential formation of tetraploid populations. Genomic confirmations of subspecies in the ecotones support the subspecies overlap predicted by the contemporary climate niche models. However, future mid-century projections of subspecies niches predict a substantial loss in range and subspecies overlap. Thus, reductions in hybridization potential could affect new recruitment of genetically variable tetraploids that are vital to this species’ ecological role. Our results underscore the importance of ecotone conservation and restoration. 
    more » « less