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 auripila group, Diptera: Cecidomyiidae) that attack three parapatric cytotypes of creosote bush (Larrea tridentata, Zygophyllaceae).

Methods: We surveyed Asphondylia species diversity at 177 sites across a 2300-km extent. After noting a correspondence between the distributions of eight Asphondylia species and L. tridentata cytotypes, we fine-mapped Asphondylia species range limits with transects spanning cytotype contact zones. We then tested whether plant-insect interactions and/or abiotic factors explain this coincidence by (1) comparing attack rates and gall midge communities on alternative cytotypes in a narrow zone of sympatry and (2) 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 6/17 Asphondylia species (including two novel putative species confirmed with COI sequencing) perfectly coincided with the contact zone of diploid and tetraploid L. tridentata. One midge species was restricted to diploid host plants while five were restricted to tetraploid and hexaploid host plants. Where diploid and tetraploid L. tridentata are sympatric, cytotype-restricted midge species more frequently attacked their typical host and Asphondylia community 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 many Asphondylia species due to plant-insect interactions. The distribution of L. tridentata cytotypes 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.

Keywords: Asphondylia; Cecidomyiidae; Larrea tridentata; North American deserts; creosote bush; gall midge; herbivory; polyploidy; species distribution models; species interactions.

Figure 1.

Map of sampling sites. (a) 177 total sites surveyed in this study. Shading shows the approximate distribution of diploid (2x), tetraploid (4x), and hexaploid (6x) L. tridentata (after Laport and Ramsey, 2015). L. tridentata cytotypes in the Lower Colorado River Valley and Baja California Peninsula have not been directly determined by flow cytometry. Arrowheads indicate transect locations. (b) Four contact zone transects. Symbols indicate creosote bush cytotype: white squares = 2x, gray circles = 4x, dark gray triangles = 6x. (c) Site of diploid–tetraploid sympatry within San Pedro transect showing location of 72 surveyed plants.

Figure 2.

Maximum likelihood phylogeny of Asphondylia auripila group inferred from cytochrome c oxidase subunit I (COI) sequences. Two novel putative species (A. sp. “acuminata” and A. sp. “hirsuta”) are indicated in bold. Number of samples per species given in parentheses. Bootstrap support values ≥ 50% are indicated above branches. Scale bar represents number of substitutions per site. Host plant use shown with symbols at right: white squares = 2x, gray circles = 4x, dark gray triangles = 6x.

Figure 3.

The range limits of six Asphondylia species and the adaxial silicula gall morphotype are concordant with the contact zone between diploid (white square) and tetraploid (gray circle) L. tridentata. For each species or morphotype, the first two columns show gall prevalence (proportion of plants with a gall) in contact zone transects. Relative position along the transect is shown on the x-axis. The third column shows gall prevalence on each plant cytotype where they naturally occur in sympatry.

Figure 4.

Non-metric multidimensional scaling (NMDS) ordination of Asphondylia communities on sympatric diploid (white square) and tetraploid (gray circle) plants. Cytotype was a significant predictor of community structure (PERMANOVA, R² = 0.33, P < 0.001)

Figure 5.

Species records and habitat suitability predictions for six cytotype-restricted species. Dark gray areas show suitable habitat when applying a 10% omission rate threshold. All species have predicted suitable habitat beyond their observed range limits. For species found on polyploid L. tridentata (all but A. sp. “acuminata”), tests of model transferability (Appendix S2) suggest species distribution models may under-predict the extent of suitable habitat in the Chihuahuan Desert. Predictions for all species except A. villosa are based on models fit using biased background sampling; A. villosa predictions are based upon predictions from spatially thinned models.