Evolution of parasitoid host preference and performance in response to an invasive host acting as evolutionary trap

The invasion of a novel host species can create a mismatch in host choice and offspring survival (performance) when native parasitoids attempt to exploit the invasive host without being able to circumvent its resistance mechanisms. Invasive hosts can therefore act as evolutionary trap reducing parasitoids’ fitness and this may eventually lead to their extinction. Yet, escape from the trap can occur when parasitoids evolve behavioural avoidance or a physiological strategy compatible with the trap host, resulting in either host-range expansion or a complete host-shift. We developed an individual based model to investigate which conditions promote parasitoids to evolve behavioural preference that matches their performance, including host-trap avoidance, and which conditions lead to adaptations to the unsuitable hosts. One important aspect of these conditions was reduced host survival during incompatible interaction, where a failed attempt by a parasitoid resulted in host killing. This non-reproductive host mortality had a strong influence on the likelihood of establishment of novel host-parasitoid relationship. Killing unsuitable hosts can constrain adaptation under conditions which in fact promoted adaptation when parasitoids would leave the trap host unharmed and survive parasitoid attack. Moreover, our model revealed that host-search efficiency and genetic variation in host-preference play a key role in the likelihood that parasitoids will include the suboptimal host in their host range, or will evolve behavioural avoidance resulting in specialization and host-range conservation, respectively. Hence, invasive species might change the evolutionarily trajectory of native parasitoid species, which is important for predicting biocontrol ability of native parasitoids towards novel hosts.

Genome-Wide SNP Analysis of Male and Female Rice Field Frogs, Hoplobatrachus rugulosus, Supports a Non-Genetic Sex Determination System

Sex determination systems (SDSs) in anurans are diverse and have undergone independent evolutionary transitions among species. The mode of sexual reproduction of the rice field frog (Hoplobatrachus rugulosus)—an economically viable, edible amphibian species—is not well known. Previous studies have proposed that threshold temperature conditions may determine sex in these frogs. To elucidate the SDS in H. rugulosus, we karyotyped 10 male and 12 female frogs, and performed fluorescence in situ hybridization combined with sequencing analyses using DArTseq™. Our results revealed a highly conserved karyotype with no sex chromosome heteromorphism, and the sequencing analyses did not identify any consistent sex-linked loci, supporting the hypothesis of temperature-dependent sex determination. The results of this study, and others, on SDSs in the rice field frog and related species also provide support for the theory that heteromorphic sex chromosomes may lead to an evolutionary trap that prevents variable SDSs. These findings add important information to the body of knowledge on H. rugulosus and are likely to have a significant impact on the productivity and economic success of rice field frog farming.

Plastic Pollution and Small Juvenile Marine Turtles: A Potential Evolutionary Trap

The ingestion of plastic by marine turtles is now reported for all species. Small juvenile turtles (including post-hatchling and oceanic juveniles) are thought to be most at risk, due to feeding preferences and overlap with areas of high plastic abundance. Their remote and dispersed life stage, however, results in limited access and assessments. Here, stranded and bycaught specimens from Queensland Australia, Pacific Ocean (PO; n = 65; 1993–2019) and Western Australia, Indian Ocean (IO; n = 56; 2015–2019) provide a unique opportunity to assess the extent of plastic (> 1mm) ingestion in five species [green (Chelonia mydas), loggerhead (Caretta caretta), hawksbill (Eretmochelys imbricata), olive ridley (Lepidochelys olivacea), and flatback turtles (Natator depressus)]. In the Pacific Ocean, high incidence of ingestion occurred in green (83%; n = 36), loggerhead (86%; n = 7), flatback (80%; n = 10) and olive ridley turtles (29%; n = 7). There was an overall lower incidence in IO; highest being in the flatback (28%; n = 18), the loggerhead (21%; n = 14) and green (9%; n = 22). No macroplastic debris ingestion was documented for hawksbill turtles in either site although sample sizes were smaller for this species (PO n = 5; IO n = 2). In the Pacific Ocean, the majority of ingested debris was made up of hard fragments (mean of all species 52%; species averages 46–97%), whereas for the Indian Ocean these were filamentous plastics (52%; 43–77%). The most abundant colour for both sites across all species was clear (PO: 36%; IO: 39%), followed by white for PO (36%) then green and blue for IO (16%; 16%). The polymers most commonly ingested by turtles in both oceans were polyethylene (PE; PO-58%; IO-39%) and polypropylene (PP; PO-20.2%; IO-23.5%). We frame the high occurrence of ingested plastic present in this marine turtle life stage as a potential evolutionary trap as they undertake their development in what are now some of the most polluted areas of the global oceans.

Plastic ingestion as an evolutionary trap: Toward a holistic understanding

Human activities are changing our environment. Along with climate change and a widespread loss of biodiversity, plastic pollution now plays a predominant role in altering ecosystems globally. Here, we review the occurrence of plastic ingestion by wildlife through evolutionary and ecological lenses and address the fundamental question of why living organisms ingest plastic. We unify evolutionary, ecological, and cognitive approaches under the evolutionary trap theory and identify three main factors that may drive plastic ingestion: (i) the availability of plastics in the environment, (ii) an individual’s acceptance threshold, and (iii) the overlap of cues given by natural foods and plastics.

Learning can be detrimental for a parasitic wasp

Animals have evolved the capacity to learn, and the conventional view is that learning allows individuals to improve foraging decisions. The parasitoid Telenomus podisi has been shown to parasitize eggs of the exotic stink bug Halyomorpha halys at the same rate as eggs of its coevolved host, Podisus maculiventris, but the parasitoid cannot complete its development in the exotic species. We hypothesized that T. podisi learns to exploit cues from this non-coevolved species, thereby increasing unsuccessful parasitism rates. We conducted bioassays to compare the responses of naïve vs. experienced parasitoids on chemical footprints left by one of the two host species. Both naïve and experienced females showed a higher response to footprints of P. maculiventris than of H. halys. Furthermore, parasitoids that gained an experience on H. halys significantly increased their residence time within the arena and the frequency of re-encounter with the area contaminated by chemical cues. Hence, our study describes detrimental learning where a parasitoid learns to associate chemical cues from an unsuitable host, potentially re-enforcing a reproductive cul-de-sac (evolutionary trap). Maladaptive learning in the T. podisi—H. halys association could have consequences for population dynamics of sympatric native and exotic host species.

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

We report a chromosome-level assembly for Pieris macdunnoughii, a North American butterfly whose involvement in an evolutionary trap imposed by an invasive Eurasian mustard has made it an emerging model system for studying maladaptation in plant–insect interactions. Assembled using nearly 100× coverage of Oxford Nanopore long reads, the contig-level assembly comprised 106 contigs totaling 316,549,294 bases, with an N50 of 5.2 Mb. We polished the assembly with PoolSeq Illumina short-read data, demonstrating for the first time the comparable performance of individual and pooled short reads as polishing data sets. Extensive synteny between the reported contig-level assembly and a published, chromosome-level assembly of the European butterfly Pieris napi allowed us to generate a pseudochromosomal assembly of 47 contigs, placing 91.1% of our 317 Mb genome into a chromosomal framework. Additionally, we found support for a Z chromosome arrangement in P. napi, showing that the fusion event leading to this rearrangement predates the split between European and North American lineages of Pieris butterflies. This genome assembly and its functional annotation lay the groundwork for future research into the genetic basis of adaptive and maladaptive egg-laying behavior by P. macdunnoughii, contributing to our understanding of the susceptibility and responses of insects to evolutionary traps.