Search bioRxiv⌕ Search

Biology subjects

Villacis-Perez, E.

Publications and source records attributed to Villacis-Perez, E..

6 recordsLinked to original sources

Hybrid breakdown is temporary and not expressed in a novel environment during 50 generations of experimental evolution in Tetranychus urticae hybrids

Hybridization, the interbreeding between species or genetically distinct populations, can lead to deleterious fitness consequences, but simultaneously it can boost adaptive potential by increasing genetic variation, especially in novel environments. However, how incompatibilities and beneficial genetic combinations interplay across generations remains poorly understood. Here, we tracked how two fitness proxies, the absolute number of adult offspring and the proportion of eggs that reached adulthood, evolve in parental and hybrid populations at three different time points over 50 generations, in both novel and ancestral environments. To test this, we used two geographically distinct populations with low divergence (Dxy=0.002) of the two-spotted spider mite (Tetranychus urticae). Across the first three generations, hybrids showed significantly lower fitness than parental populations in the ancestral environment, indicating incompatibilities between the parental genomes. In contrast, hybrid and parental fitnesses were similar in the novel environment, indicating that the impact of incompatibilities was minor compared to the selection imposed by the novel environment. However, after 50 generations, hybrids displayed similar fitness relative to parental populations in all environments, suggesting resolution of the incompatibilities. Furthermore, around generation 45, hybrids temporarily outperformed parental populations in a novel environment, suggesting a transient window of higher adaptive potential, before fitness stabilized again by generation 50. In conclusion, we show that hybrid populations of T. urticae can swiftly purge incompatibilities when genetic divergence is low. These findings suggest that the dynamics of incompatibility resolution and adaptive potential of novel haplotypes play out over a long time frame, highlighting the importance of tracking hybrid fitness past the first few generations.

evolutionary biology↗

Genome sequence and efficient CRISPR/Cas9 gene editing in the solanacea specialist pest Tetranychus evansi

Tetranychus evansi is an invasive spider mite pest of solanaceous crops worldwide. Its global expansion and ability to rapidly develop acaricide resistance highlight the need for robust genomic resources and functional genetic tools to design custom control strategies. Here, we deliver a high-quality genome assembly and establish efficient CRISPR/Cas9 editing in T. evansi to enable mechanistic studies of host adaptation and pesticide resistance. Using an inbred line and Oxford Nanopore Technologies (ONT) long-read sequencing ([~]36x), we assembled an 89 Mb genome into 13 contigs (N50 = 18.6 Mb) with high completeness and annotated 14,246 protein-coding genes. We manually curated the principal detoxification gene families (P450s, CCEs, GSTs, UGTs, ABC transporters and DOGs), revealing consistently smaller repertoires than in the highly polyphagous relative Tetranychus urticae. To enable reverse genetics, we adapted SYNCAS (saponin + branched amphiphilic peptide capsules) for maternal delivery of CRISPR/Cas9 in T. evansi. Targeting the phytoene desaturase (PD) pigmentation marker produced reliable knockouts with visible albinism and mean editing efficiencies of [~]9.6-14.7%, allowing establishment of stable mutant lines. We further applied precision gene editing to knock-in (KI) the M918T and M918L substitutions into the voltage-gated sodium channel (VGSC). While M918L was lethal in T. evansi, we generated multiple homozygous lines for M918T (mean KI [~]4.4%). Bioassays demonstrated that while the mutation caused extremely high levels of bifenthrin resistance (RR>1000), this was less so for cyfluthrin (RR=164), revealing the independent and specific role of M918T in pyrethroid resistance. Collectively, these resources establish T. evansi as a tractable system for reverse genetic analysis and provide a reference for future comparative and population genomics.

genetics↗

Genetic and phenotypic variation between Tetranychus ludeni populations from Benelux

The occurrence of the bean spider mite, Tetranychus ludeni, in The Netherlands and Belgium is reported here for the first time. Mite populations were collected from the field and established in the laboratory. Morphological and genetic analyses were performed to determine the species identity of multiple field-collected individuals. Comparing the sequence of the mitochondrial cytochrome oxidase subunit-1 (CO1) of the field populations with sequences available in NCBI revealed the extent of genetic differentiation between T. ludeni populations from around the world. The reproductive performance of mated females was assessed on various host plant species relevant to agriculture, including several leguminous species and tomato. These findings highlight the potential of T. ludeni to become an agricultural pest in Europe, particularly in the context of increasing global temperatures and agricultural practices.

evolutionary biology↗

Independent genetic mapping experiments identify diverse molecular determinants of host adaptation in a generalist herbivore

Interactions between plants and herbivores promote evolutionary change. Studying the evolution of herbivore mechanisms aimed to cope with diUerent host plant species is a critical intersection between evolutionary biology and sustainable pest management. Generalist herbivores are of particular interest, as hybridization between genetically distinct populations can increase the standing genetic variation and therefore the adaptive potential of the species. Tetranychus urticae is a generalist arthropod known for its adaptive potential, evidenced in its immense host range and ability to develop metabolic resistance to xenobiotics. However, the molecular underpinnings associated with the potential of host adaptation and the consequences of host adaptation in this and many other pests remain elusive. Here, we use two independent, empirical approaches to identify and map the genetic basis of host plant performance and adaptation in genetically distinct populations of T. urticae. In the first approach, we subject a genetically diverse mite population to tomato selection and map genomic regions linked to the phenotypic evolution of increased reproductive performance. In the second approach, we map genomic regions responsible for performance on tomato by comparing the genomes of pooled individuals from a F2 backcross between populations with high and low reproductive performance. Both approaches revealed specific and shared genomic regions associated with host plant performance and adaptation and key candidate genes were identified. Our findings highlight the power of spider mite genetic approaches to identify the complex genetic basis of host adaptation in a generalist herbivore.

evolutionary biology↗

Competitor Displacement by an Herbivore that Manipulates Plant Defences

Tetranychus evansi is an herbivorous mite specialised on solanaceous hosts, although it has also been observed to colonise non-solanaceous species. It has the ability to suppress the defences of tomato (Solanum lycopersicum), and it can displace competitors from this host using a diverse array of traits. T. evansi is an invasive species in Africa and Europe, where it often displaces native species. While recent evidence suggests that T. evansi can also suppress defences of non-solanaceous hosts, there is a lack of understanding of the molecular changes induced upon mite infestation on hosts other than tomato, as well as how these changes may impact populations of competing herbivores. Here, we investigate the transcriptomic and metabolomic responses of bean (Phaseolus vulgaris) to T. evansi infestation and to T. urticae infestation, a cosmopolitan congeneric that often competes with T. evansi for hosts in areas of co-occurrence. We ask whether the presence of T. evansi facilitates bean colonization for T. urticae, and whether the spatial distribution of mite feeding sites depends on the presence of competitors on bean leaves. We examine whether this facilitation is attributed to jasmonic acid (JA) or salicylic acid (SA) defences by treating plants with exogenous SA and JA and comparing the transcriptomes and metabolomes of bean exposed to either phytohormones or to mite feeding. Finally, we measure phytohormone concentrations and the expression of JA- and SA-responsive genes in plants infested with either mite species or co-infested with both, at different spatial scales. We found that, as previously observed on tomato, T. urticae benefits from the suppression of bean defences when sharing a leaf with T. evansi. Phytohormone treatments revealed that the reproductive performance of both species decreases with artificially induced JA defences, irrespective of the presence of SA. We found that the molecular suppression and induction of defences is mostly, but not exclusively restricted to the leaf area from where the mites feed. In full leaves co-infested with both mites, levels of marker gene induction were comparable to the inducer mite T. urticae, although not as prominent, while in smaller feeding arenas where both species fed closely to each other, the expression of a JA-responsive proteinase inhibitor was suppressed. When residing alone on a leaf, both mites had distinct preferred feeding sites with only partial overlap, but when sharing a leaf, T. evansi retained its preferred feeding site and T. urticae moved away from its own. We argue that the suppression of defences by T. evansi is mostly, although not exclusively, locally restricted, and thus the spatial distribution of individuals on the leaf is a strong determinant of competitor facilitation. This suggests that traits that displace competitors from plant tissues with suppressed defences would be under selection to co-evolve together with defence suppression.

ecology↗

Intraspecific diversity in the mechanisms underlying abamectin resistance in a cosmopolitan pest

Pesticide resistance relies on a myriad of mechanisms, ranging from single mutations to a complex and polygenic architecture, and it involves mechanisms such as target-site insensitivity, metabolic detoxification, or a combination of these, with either additive or synergistic effects. Several resistance mechanisms against abamectin, a macrocyclic lactone widely used in crop protection, have been reported in the cosmopolitan pest Tetranychus urticae. However, it has been shown that a single mechanism cannot account for the high levels of abamectin resistance found across different mite populations. Here, we used experimental evolution combined with bulked segregant analyses to map quantitative trait loci (QTL) associated with abamectin resistance in two genetically unrelated strains of T. urticae. In these two independent QTL mapping experiments, three and four QTLs were identified, of which three were shared between experiments. Shared QTLs contained genes encoding subunits of the glutamate-gated chloride channel (GluCl) and harboured previously reported mutations, including G314D in GluCl1 and G326E in GluCl3, but also novel resistance candidate loci, including DNA helicases and chemosensory receptors. Surprisingly, the fourth QTL, present only in only one of the experiments and thus unique for one parental resistant strain, revealed a non-functional variant of GluCl2, suggesting gene knock-out as resistance mechanism. Our study uncovers the complex basis of abamectin resistance, and it highlights the intraspecific diversity of genetic mechanisms underlying resistance in a cosmopolitan pest.

molecular biology↗