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Spatial sorting promotes rapid (mal)adaptation in the red-shouldered soapberry bug after hurricane-driven local extinctions

Nature Ecology & Evolution volume 7, pages 1856–1868 (2023)Cite this article

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Abstract

Predicting future evolutionary change is a critical challenge in the Anthropocene as geographic range shifts and local extinction emerge as hallmarks of planetary change. Hence, spatial sorting—a driver of rapid evolution in which dispersal-associated traits accumulate along expanding range edges and within recolonized habitats—might be of growing importance in ecology and conservation. We report on the results of a natural experiment that monitored recolonization of host plants by the seed-feeding, red-shouldered soapberry bug, Jadera haematoloma, after local extinctions from catastrophic flooding in an extreme hurricane. We tested the contribution of spatial sorting to generate rapid and persistent evolution in dispersal traits, as well as in feeding traits unrelated to dispersal. Long-winged dispersal forms accumulated in recolonized habitats and due to genetic correlation, mouthparts also became longer and this shift persisted across generations. Those longer mouthparts were probably adaptive on one host plant species but maladaptive on two others based on matching the optimum depth of seeds within their host fruits. Moreover, spatial sorting eroded recently evolved adaptive divergence in mouthpart length among all host-associated biotypes, an outcome pointing to profound practical consequences of the extreme weather event for local adaptation, population resilience and evolutionary futures.

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Fig. 1: Hurricane-associated flooding.
Fig. 2: Soapberry bug morphology and host plants.
Fig. 3: The effect of hurricane-associated flooding on soapberry bug population size and egg survival.
Fig. 4: Spatial sorting shifts the frequency of macropterous soapberry bugs.
Fig. 5: Spatial sorting promotes shifts in soapberry bug beak lengths.
Fig. 6: Spatial sorting erodes the history of host-associated natural selection.

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Data availability

All data collected for this project are freely available in the digital repository Dryad: https://doi.org/10.5061/dryad.tht76hf4t.

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Acknowledgements

We acknowledge funding by the American Museum of Natural History’s Teddy Roosevelt grant to M.S.C., the American Philosophical Society’s Lewis and Clark Explorer grant and the Society for the Study of Evolution’s Small Grants for Local and Regional Outreach and funding to S.P.E. and S.P.C. from the National Science Foundation (award no. 1802715). We thank NSF programme officer G. Gilchrist for his critical feedback during the planning stages of this RAPID funded project. We thank J. Pawell for her integral role in insect field collections along with M. Comerford, R. LaRoche, L. Zhang and K. Gonzalez. In addition, we thank C. Boschert, K. Zhu, B. Ma and L. Ivanov for their contribution in measuring insect morphology. We would also like to extend a special thank you to C. Klein and her autumn 2018 Environmental Science class at Westside High School in Houston ISD for granting us access to Wolf Prairie and for their participation in this research. Artwork of insects interacting with host seed pods was done by T. M. Fowels.

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Authors and Affiliations

  1. Department of BioSciences, Rice University, Houston, TX, USA

    Mattheau S. Comerford, Tatum M. La & Scott P. Egan

  2. Clements High School, Sugar Land, TX, USA

    Tatum M. La

  3. Department of Entomology & Nematology, University of California, Davis, CA, USA

    Scott Carroll

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  1. Mattheau S. Comerford
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  2. Tatum M. La
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  4. Scott P. Egan
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Contributions

The focus of this paper was conceived by M.S.C., S.C. and S.P.E. Data collection was performed by M.S.C. and T.M.L. with analysis by M.S.C. Writing was shared by M.S.C. and S.P.E. with feedback from S.C. and T.M.L.

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Correspondence to Mattheau S. Comerford.

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Extended data

Extended Data Fig. 1 Map of sample sites in this study.

Map of soapberry bug sample sites by host association across Houston, Texas, U.S.A., from 2017 to 2020. Open circles denote unflooded control sites and filled circles denote flooded site locations. Host association is depicted by colour: Koelreuteria (blue), Sapindus (orange) and Cardiospermum (green). For corresponding latitude and longitude of each sample site location see Supplementary Table 1.

Extended Data Fig. 2 Wing and beak lengths across multiple generations.

Boxplot showing soapberry bug wing and beak lengths across multiple generations of Koelreuteria-associated brachypterous females. Panel (a) is a generational comparison of insect wing length between flooded (dark blue) and unflooded control sites (light blue). Model selection using linear mixed models (LMM) suggests that forewing lengths were longer at flooded sites in the three generations that followed recolonization (LMM: F(3, 205.1) = 10.80, P < 0.001; Supplementary Table 5). Panel (b) is a generational comparison of insect beak length between flooded (dark blue) and unflooded control sites (light blue). Model selection using LMM suggests that beak lengths were longer at flooded sites in the three generations that followed recolonization (LMM: F(3, 202.6) = 27.44, P < 0.001; Supplementary Table 14). In both panels, the red dashed line corresponds to Hurricane Harvey. Each ‘generation’ represents a 60-day block of time, which is equivalent to the maximum adult lifespan of a soapberry bug50. The upper and lower edges of the box indicate the first and third quartile, the midline indicates the median value and the whiskers show the 95% confidence intervals with dots as outliers. Sample sizes in grey within panels. Boxes capped with different letters are significantly different (Tukey’s test: P < 0.05, see Supplementary Tables 15, 22). There were no brachypterous insects present during initial colonization, so a boxplot for flooded post-hurricane insects was not included in either panel.

Extended Data Fig. 3 Pre-hurricane regional patterns of soapberry bug beak length.

Boxplot summarizing regional patterns of beak length in soapberry bugs sampled before the hurricane separated by sex (male and female) and wing form (macropterous insects in orange and brachypterous insects in blue). Model selection using linear mixed models suggests that females have longer beaks than males and macropterous individuals have longer beaks than brachypterous individuals (LMM: F(1, 1079.) = 18.286, P < 0.001; Supplementary Table 6) The upper and lower edges of each box indicate the first and third quartile, the midline indicates the median value and the whiskers show the 95% confidences intervals with dots as outliers. Box plots labelled with different letters are significantly different (Tukey’s test: P < 0.01, see Supplementary Table 23). Sample sizes provided in grey below each boxplot.

Extended Data Fig. 4 Soapberry bug beak length before and after hurricane.

Line plots illustrating hurricane-associated beak length changes of soapberry bugs at flooded (left) and control sites (right). Insect beak lengths are compared pre- and post-hurricane with the pink column in the middle marking the timing of Hurricane Harvey. Each coloured line represents an individual sampling site. The colour of each line represents the host association with Cardiospermum (green), Sapindus (orange) and Koelreuteria (blue). Box plots on left (pre-hurricane) and right (post-hurricane) illustrate the overall median, first and third quartile, 95% confidence intervals and outliers. Bars with asterisk indicate levels of significance per two-tailed Welch’s test with (*) <0.05 and (***) <0.001, with test statistics provided at the top of each panel. Sample sizes in grey. Plots are aligned by horizontally by sex and wing form to account for previously demonstrated dimorphic differences in beak length (see Extended Data Fig. 3).

Extended Data Fig. 5 Host plant-associated beak length before hurricane.

Boxplot of host-associated beak lengths from soapberry bugs collected before the hurricane. Insect beak lengths are compared between host association denoted by colour with Cardiospermum (green), Koelreuteria (blue) and Sapindus (orange) and separated by sex (females – top; males – bottom) and wing form (macropterous – left; brachypterous – right; see Extended Data Fig. 3). Model selection using linear mixed models suggest that sex, wing form and host association are all important predictors of insect beak length (LMM: F (2, 1079) = 2.88, P = 0.057; Supplementary Table 16). The upper and lower boxes indicate the first and third quartile, the midline indicates the median value and the whiskers show the 95% confidence intervals with dots as outliers. Boxes labelled with different letters are significantly different (Tukey’s test: P < 0.05, see Supplementary Table 17). Sample sizes in grey within panels.

Extended Data Fig. 6 Beak length before and after hurricane for macropterous soapberry bugs.

Boxplot of spatial sorting’s effect on eroding a history of natural selection driven host-associated beak length differentiation in macropterous soapberry bugs. Divergent host-associated beak lengths (s ee Extended Data Fig. 5) are compared pre- (white) versus post-hurricane (purple). Insect host association is denoted by images of the insect feeding on each of their given host plants: Cardiospermum (green), Koelreuteria (red) and Sapindus (orange). Model selection using linear mixed models found the three-way interaction to be significant (LMM: F(1, 518.5) = 22.88, P < 0.001; Supplementary Table 24), however, a post hoc Tukey’s test suggests that host-associated beak lengths where no longer significantly different post-hurricane at the flooded sites (Tukey: P > 0.1). All Sapindus-associated sites flooded during the hurricane, so none were available in controls. Plots are aligned vertically by site condition with flooded sites on the left and unflooded control sites on the right. Plots are aligned horizontally by sex with females on the top and males on the bottom. The upper and lower edge of box plots indicate the first and third quartile, the midline indicates the median value and the whiskers show the 95% confidences intervals with dots as outliers. Boxes labelled with different letters are significantly different (Tukey’s test: P < 0.05). Sample sizes in grey included in panels.

Extended Data Fig. 7 Beak length before and after hurricane for brachypterous soapberry bugs.

Boxplot of spatial sorting’s effect on eroding a history of natural selection driven host-associated beak length differentiation in brachypterous soapberry bugs. Divergent host-associated beak lengths (See Extended Data Fig. 5) are compared pre- (white) versus post-hurricane (light blue). Insect host association is denoted by images of the insect feeding on each of their given host plants: Cardiospermum (green), Koelreuteria (red) and Sapindus (orange). Model selection using linear models found the three-way interaction to be significant (LM: F(1, 509) = 4.12, P = 0.04; Supplementary Table 25), however, post hoc Tukey’s test suggests that that host-associated differences between beak lengths are no longer significant at flooded sites post-hurricane (Tukey: P > 0.1). All Sapindus-associated sites flooded during the hurricane, so none were available in controls. Plots are aligned vertically by site condition with flooded sites on the left and unflooded control sites on the right. Plots are aligned horizontally by sex with females on the top and males on the bottom. The upper and lower edge of box plots indicate the first and third quartile, the midline indicates the median value and the whiskers show the 95% confidence intervals with dots as outliers. Boxes labelled with different letters are significantly different (Tukey’s test: P < 0.05). Sample sizes in grey included in panels.

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Comerford, M.S., La, T.M., Carroll, S. et al. Spatial sorting promotes rapid (mal)adaptation in the red-shouldered soapberry bug after hurricane-driven local extinctions. Nat Ecol Evol 7, 1856–1868 (2023). https://doi.org/10.1038/s41559-023-02205-7

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