DOI: 10.5061/dryad.tht76hf4t
title: Spatial sorting promotes rapid (mal)adaptation in the red-shouldered soapberry bug after hurricane-driven local extinctions

description: 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 re-colonization 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
 re-colonized habitats, and due to genetic correlation, mouthparts also
 became longer, and this shift persisted across generations. Those longer
 mouthparts were likely 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.
description: Field sampling soapberry bug populations Our
 study was conducted as a long-term natural experiment in a 1,200
 km<sup>2</sup> region in the Houston area that spanned the
 year prior to and the three years after the 2017 flooding event caused by
 Hurricane Harvey. In doing so, we monitored soapberry bug populations that
 inhabit three locally available host plant species, balloon vine
 (<em>Cardiospermum</em> <em>halicacabum</em>),
 western soapberry (<em>Sapindus</em> v.
 <em>drummondii</em>), and goldenrain tree
 (<em>Koelreuteria</em> <em>elegans</em>), (Fig.
 2d-f). Our study included 15 sites (three <em>C.
 halicacabum</em>, three <em>S</em>.
 <em>drummondii</em>, and nine <em>K. elegans</em>;
 Extended Figure 1) sampled 72 times over the three-year period after the
 hurricane (September 2017 to September 2020). Sampling was performed on
 days without precipitation and was conducted between the hours of 10:00
 and 15:00. Each site was sampled once every 14 days. Of the 15 monitored
 sites, nine sites flooded (three <em>S. drummondii</em>,
 six<em> K. elegans</em>,<em> </em>two<em> C.
 halicacabum</em>), while four sites did not flood and serve as our
 controls (three <em>K. elegans</em> and one
 <em>C</em>. <em>halicacabum</em>; Supplemental
 Table 1). Flooded sites in this study were inundated with standing water
 from 7 days to 90+ days. No <em>S</em>.
 <em>drummondii</em> sites were included in our control as this
 natural experiment relied on the serendipitous overlap of flood patterns
 with our previous history of insect sampling. Taking advantage of
 haphazard flooding also created discrepancies in host plant abundance,
 which varied between sampling site with <em>Koelreuteria</em>-
 and <em>Sapindus</em>-associated sites consisting of anywhere
 from one to seven trees and Cardiospermum-associated sites consisting of
 five to twenty herbaceous plants. For each sampling
 effort, insects were collected by hand over a period of 30 minutes from a
 50 m<sup>2</sup> region around the base of the host plant.
 Captured insects were temporarily stored in a plastic container lined with
 Insect-a-Slip (polytetrafluoroethylene coating, Bio Quip Products, Inc.,
 Rancho Dominguez, CA). For each individual soapberry bug, insect
 beak-length was measured in the field using a digital caliper (Stainless
 Steel iGaging ABSOLUTE ORIGIN 0–6ʺ Digital LCD Electronic Caliper-IP54;
 iGaging, Los Angeles, Calif.), and wing morphology (macropterous = full
 flight wings; brachypterous = reduced wings) was visually assessed by the
 presence of developed corium of the distal membrane of the insect’s
 forewing (Fig. 2b). Captured insects were immediately returned to their
 habitat after morphological measurements to avoid artificial selection on
 any population. Given that some flooded sites were colonized earlier than
 others, we limited our data analysis to individuals collected in the first
 year (26 sampling periods) after colonization at flooded sites and after
 the hurricane at control sites to avoid overrepresentation of any one
 individual site.  Field measurements of soapberry bug
 morphology The morphological measurements of the focal
 insect traits included beak length, wing-form, and insect forewing length.
 We measured beak length as the distance from the clypeus margin of the
 insect's lower sclerites to the most distal point of the labium. The
 categorical variable wing-form was determined to be either “brachypterous”
 or “macropterous” based on visual inspection. An individual was classified
 as brachypterous when the medio-cubital and apical folding fields of the
 hind wing were underdeveloped and a developed distal membrane on forewing
 was absent; an individual was classified to be “macropterous” if the
 medio-cubital and apical folding fields of the hindwing were fully
 developed and the distal membrane of the forewing was present (Fig. 2b,c).
 Forewing length was measured as the distance from the proximal margin of
 the scutellum to the distal edge of the forewing membrane. Individuals
 where trait measurements were obscured by damage were excluded. 
description: This data was entered in Excel, and analysis was conducted in
 R.
description: # Title of data set Spatial sorting promotes rapid (mal)adaptation in the
 red-shouldered soapberry bug after hurricane-driven local extinctions ##
 Description of the data and file structure This is a data file of Jadera
 haematoloma phenotypic trait shifts in response to hurricane-associated
 spatial sorting in Houston TX, USA The data has 11 columns and 3688 rows.
 Each row represents a unique insect sampled during the three-year
 experiment. C Column A [Site] is the official sample site name provided in
 the manuscript. Site is used as a random effect in most models to account
 for site level variation. Column B [Step] is the sample time relevant to
 Hurricane Harvey with negative numbers being pre-hurricane and positive
 numbers being post-hurricane. Each sampling period represents a two week
 increment of time. Column C [Host] this column indicates the
 host-association of each insect sampled Cardiospermum, Sapindus, and
 Koelreuteria. Column D [Wing\_form] is the wing form of each insect with
 L= large winged macropterous insects and S= small winged brachypterous
 insects Column E [sex] is the sex of each insect sampled, with F = female,
 and M = male Column F [Beak] the length in mm of the insects mouthparts
 Column G [Wing] The wing length in mm of the insect Column H [Type] is the
 site condition relative to the hurricane: control = non-flooded sites,
 flooded = sites that flooded and led to local extinction event Column I
 [Time] this is the collection time relative to the hurricane: pre= before
 hurricane, post= after hurricane ## Sharing/Access information To access
 this data or ask questions related to the data you may contact Mattheau
 Comerford via email at mattheauc@gmail.com