Pre‐ and post‐ingestive defenses affect larval feeding on a lethal invasive host plant

Abstract

Evolutionary traps arise when organisms use novel, low‐quality or even lethal resources based on previously reliable cues. Persistence of such maladaptive interactions depends not only on how individuals locate important resources, such as host plants, but also the mechanisms underlying poor performance. Pieris macdunnoughii (Remington) (Lepidoptera: Pieridae) lays eggs on a non‐native mustard, Thlaspi arvense (L.) (Brassicaceae), which is lethal to the larvae. We first tested whether larval feeding behavior was affected before (pre‐) ingestion or following (post‐) ingestion of leaf material, indicating activity of feeding deterrents, toxins, or both in this evolutionary trap. Neonates were less likely to start feeding and eventually fed more slowly on T. arvense than on the native host plant Cardamine cordifolia (Gray) (Brassicaceae) in both laboratory and field. Starvation was a primary cause of mortality, indicating the role of a feeding deterrent. Feeding did not differ between larvae from invaded and uninvaded population. Second, T. arvense defensive chemistry is dominated by the glucosinolate sinigrin (allyl or 2‐propenyl glucosinolate). Adding sinigrin to the leaves of T. arvense and native hosts C. cordifolia and Descurainia incana (Bernhardi ex Fischer & Meyer) (Brassicaceae) delayed the onset of feeding, caused larvae to feed more slowly, and decreased survival on the native hosts. This evolutionary trap may not be driven by a novel deterrent, but rather by a change in the concentration of a deterrent found in native hosts. Many insects have adapted to evolutionary traps posed by invasive plants, incorporating the new plant into their diets. Thlaspi arvense remains lethal to P. macdunnoughii, and pre‐ingestive deterrents such as excess sinigrin may contribute to persistent maladaptation.

Host plant diet affects growth and induces altered gene expression and microbiome composition in the wood white (Leptidea sinapis) butterfly

“…Consequently, butterflies that overcome the recognition and detoxification barriers associated with novel host plant use may enter an unexplored "adaptive realm", which could lead to comparatively rapid diversification, if the novel host plant is part of a diverse plant lineage where most species have similar chemical composition (Ehrlich & Raven, 1964;Janz, 2011). Host plant expansions can also result in so-called (eco)evolutionary traps, when adult female butterflies start to prefer invasive or anthropogenic plant species for egg-laying that are suboptimal for larval development or survival (Singer & Parmesan, 2018;Steward et al, 2019).…”

“…Insects feeding on plants (phytophagous) are generally specialized on particular species or groups of host plants (Ehrlich & Raven, 1964;Janz, 2011). This can be a result of genetic, physiological, ecological and geographical restrictions in the specialists (Schoonhoven et al, 2005;Steward et al, 2019;Weingartner et al, 2006) and, crucially, the ability to overcome host plant defence mechanisms involving toxic metabolites (Ehrlich & Raven, 1964;Govind et al, 2010;Kirsch et al, 2011). Female butterflies generally identify the appropriate host plant species via chemoreception.…”

Experience may outweigh cue similarity in maintaining a persistent host‐plant‐based evolutionary trap

“…These butterflies oviposit on the invasive Eurasian species Thlaspi arvense L. (Chew 1977, Nakajima et al 2013. However, T. arvense is completely lethal to P. macdunnoughii larvae: no larvae raised on a diet of T. arvense in the lab or field survive past the pupal stage (Chew 1975, Nakajima et al 2013, Steward et al 2019. Co-occurrence with T. arvense in one field setting has been estimated to reduce fitness of ovipositing females by around 3% based on larval survival, habitat occupancy by females, and the distribution and abundance of the lethal nonnative in relation to other hosts (Nakajima et al 2013, Nakajima andBoggs 2015).…”

The Genome of the Margined White Butterfly (Pieris macdunnoughii): Sex Chromosome Insights and the Power of Polishing with PoolSeq Data

“…This montane butterfly ranges across the southern Rocky Mountains and is a hostplant specialist, laying eggs and feeding upon plants in the Brassicaceae. Importantly, it is the focus of ongoing research into how specialization has resulted in maladaptive interactions with invasive Eurasian mustards, wherein females oviposit on invasive plants despite their lethality to caterpillars ( Chew 1975 , 1977 ; Nakajima et al 2013 ; Nakajima and Boggs 2015 ; Steward and Boggs 2020 ; Steward et al 2019 ). Given the extensive literature investigating interactions between Pieris species and their hostplants, and advances in understand these interactions at the genomic level ( Edger et al 2015 ), developing a functional genomics understanding of these interactions in a species, such as P. macdunnoughii is a logical next step, but one that is hindered by the lack of genomic resources for this species.…”