A test of adaptive divergence in a newly discovered host association of the soapberry bug Jadera haematoloma on Mexican buckeye, Ungnadia speciosa

Abstract

Host races represent an important step in the speciation process of phytophagous insects as they reflect the maintenance of genetically divergent host‐associated populations in the face of appreciable gene flow. The red‐shouldered soapberry bug, Jadera haematoloma (Herrich‐Schäffer) (Hemiptera: Rhopalidae), is an oligophagous seed predator with a history of host race evolution on plant associations in the (soapberry) family Sapindaceae. Soapberry bugs are a model group for understanding rapid ecological adaptation to their hosts, and hence good candidates for investigating evolutionary divergence in host associations over short timescales. Here, we describe the recent discovery of Mexican buckeye, Ungnadia speciosa Endl., as a host of J. haematoloma in a region of the Chihuahuan desert including west Texas and southeastern New Mexico, USA. This host differs from J. haematoloma’s previously recorded hosts in the Sapindaceae in seed chemistry, ecology, and phylogeny. The tendency toward rapid, host‐associated adaptations by populations of J. haematoloma and the unique biology of the newly discovered Ungnadia host create the opportunity for potential host race formation, as it overlaps geographically with two previously recorded host plants in this region – the native western soapberry tree, Sapindus saponaria var. drummondii (Hook & Arn.), and the non‐native goldenrain tree, Koelreuteria paniculata Laxm. We explore the possibility of host race formation on Ungnadia‐associated insects by testing for host‐associated differentiation in morphology and feeding behaviors. We find evidence of differentiation in the length of the mouth parts, which is an ecologically relevant feeding trait between host plant species with larger or smaller seed capsules. This divergence is maintained in the face of potential gene flow by reproductive isolation in the form of habitat isolation, which we detect in host preference trials. Together, our results demonstrate that soapberry bugs associated with this newly discovered host exhibit morphological and behavioral traits consistent with host race formation, but additional work is required to confirm its state along the speciation continuum.

Multiple mechanisms contribute to isolation-by-environment in the redheaded pine sawfly, Neodiprion lecontei

“…Rapid phenotypic adaptation to host plants has also been documented in other insect systems (e.g., Singer et al 1993;Thompson 1998;Sousa et al 2019), often following introduction of pest insects or of novel host plants. For example, within the past 50-80 years, several host races of the American soapberry bug (Jadera haematoloma) have evolved, with the mouthpart ("beak") length corresponding to the size of the host's fruit (Carroll & Boyd, 1992;Comerford et al, 2022). These host races also have faster development time and greater survival on their novel hosts (Carroll et al, 1997(Carroll et al, , 1998.…”

Fundamental and specialized questions on host race formation and speciation – an introduction

“…(Sapindaceae), represents a host shift to a species with highly dissimilar biology to previously recorded hosts. Comerford et al (2022) tested for corresponding changes in morphology and behavior and found differentiation in mouth parts, reflecting changes in feeding traits. Herbivorous insects must be able to contend with the chemical defenses of their plant.…”

Asymmetric local adaptation to host plants (Cirsium spp.) by the phytophagous ladybird beetle Henosepilachna niponica and its implications

“…The evolution of host plant specialization is often related to the geographic heterogeneity of host plant distribution and abundance (Fox & Morrow, 1981; Thompson, 1994; Kuussaari et al., 2000; Janz & Nylin, 2008; Augustyn et al., 2017). Given that respective phytophagous specialists occasionally occupy multiple areas dominated by different host varieties, the geographic heterogeneity of host resources can promote the divergence of host specificity even within a phytophagous specialist (e.g., Stireman et al., 2005; Logarzo et al., 2011; Bagley et al., 2017; Comerford et al., 2022).…”