Phylogenomic analysis provides diagnostic tools for the identification of Anastrepha fraterculus (Diptera: Tephritidae) species complex

Abstract

Insect pests cause tremendous impact to agriculture worldwide. Species identification is crucial for implementing appropriate measures of pest control but can be challenging in closely related species. True fruit flies of the genus Anastrepha Schiner (Diptera: Tephritidae) include some of the most serious agricultural pests in the Americas, with the Anastrepha fraterculus (Wiedemann) complex being one of the most important due to its extreme polyphagy and wide distribution across most of the New World tropics and subtropics. The eight morphotypes described for this complex as well as other closely related species are classified in the fraterculus species group, whose evolutionary relationships are unresolved due to incomplete lineage sorting and introgression. We performed multifaceted phylogenomic approaches using thousands of genes to unravel the evolutionary relationships within the A. fraterculus complex to provide a baseline for molecular diagnosis of these pests. We used a methodology that accommodates variable sources of data (transcriptome, genome, and whole‐genome shotgun sequencing) and developed a tool to align and filter orthologs, generating reliable datasets for phylogenetic studies. We inferred 3031 gene trees that displayed high levels of discordance. Nevertheless, the topologies of the inferred coalescent species trees were consistent across methods and datasets, except for one lineage in the A. fraterculus complex. Furthermore, network analysis indicated introgression across lineages in the fraterculus group. We present a robust phylogeny of the group that provides insights into the intricate patterns of evolution of the A. fraterculus complex supporting the hypothesis that this complex is an assemblage of closely related cryptic lineages that have evolved under interspecific gene flow. Despite this complex evolutionary scenario, our subsampling analysis revealed that a set of as few as 80 loci has a similar phylogenetic resolution as the genome‐scale dataset, offering a foundation to develop more efficient diagnostic tools in this species group.

Molecular evolution and genetic diversity of defective chorion 1 in Anastrepha fraterculus and Anastrepha obliqua (Diptera, Tephritidae)

“…, 2012; Hernández-Ortiz et al, 2015). Although we did not investigate different morphotypes in this study that would enable us to compare these taxa to the ones described elsewhere (Hernández-Ortiz et al, 2015; Prezotto et al, 2019), the topology we found is remarkably similar to what has been described using transcriptomic and genomic data(Congrains et al, 2021;Congrains et al, 2023), which identi ed three distinct branches for A. fraterculus while supporting a single A. obliqua branch. These diverse A. fraterculus lineages may be subject to distinct selective pressures(Smith-Caldas et al, 2001;Manni et al, 2015), despite their recent divergence.…”

“…While there is evidence of pre-and postzygotic isolation among some sympatric and allopatric populations of Anastrepha species (Selivon et al, 2005;Vera et al, 2006;Rull et al, 2018), hybridization between A. fraterculus and A. obliqua has successfully produced viable offspring in the laboratory, though following Haldane's rule (Santos et al, 2001). This nding has been corroborated by population studies that indicate gene ow between these species, despite the presence of reproductive barriers (Díaz et al, 2018;Scully et al, 2018;Congrains et al, 2021;Congrains et al, 2023). In this scenario, it is possible that different parts of the genome may introgress differently, so genes with speci c reproductive biases may play a crucial role in differentiation and speciation, making their study of particular relevance for understanding the underlying forces separating Anastrepha species.…”

“…The most internal branch included all A. obliqua and two samples of A. fraterculus from central Brazil, which we will refer to as the A. fraterculus Clade VII branch. We will refer to these different A. fraterculus clades by names that loosely correspond to branches that seem to match the phylogenetic and geographic location of said branches in samples from another study (Congrains et al, 2023). This group was sister to other specimens that form the A. obliqua branch, which is generally distributed in southern and central Brazil and is related to A. ludens.…”

“…The "Anastrepha" dataset was composed of 31 sequences derived from fragments of the third exon of dec-1 ampli ed from natural populations of A. obliqua and A. fraterculus (Table 1), which belong to the two most important branches in the fraterculus group (Congrains et al, 2023), as well as dec-1 sequences from A. ludens and A. grandis. The latter was included as an outgroup.…”

“…Furthermore, these genes can serve as markers in the context of species differentiation amid phylogenetic uncertainties. Remarkably, dec-1 produces adequate phylogenetic signals at different evolutionary levels across Tephritidae, but it seems to distinguish among different lineages of A. fraterculus for which there are only a handful of informative markers, despite the plethora of genes investigated (Congrains et al, 2021;Congrains et al, 2023). Understanding its structure, isoforms, and evolutionary patterns across broader sampling also sets the stage for its establishment as a viable adequate marker to study variation across Anastrepha.…”