Genomics and ecological modelling clarify species integrity in a confusing group of butterflies

Abstract

Recent advances in both genomics and ecological modelling present new, multidisciplinary opportunities for resolving species boundaries and understanding the mechanisms that maintain their integrity in regions of contact. Here, we use a combination of high-throughput DNA sequencing and ecological niche modelling to resolve species boundaries and niche divergence within the Speyeria atlantis-hesperis (Lepidoptera: Nymphalidae) complex, a confusing group of North American butterflies. This complex is notorious for its muddled species delimitations, morphological ambiguity, and extensive mitonuclear discordance. Our admixture and multispecies coalescent-based analyses of single nucleotide polymorphisms identified substantial divergences between S. atlantis and S. hesperis in areas of contact, as well as between distinct northern and southern lineages within S. hesperis. Our results also provide evidence of past introgression relating to another species, S. zerene, which previous work has shown to be more distantly related to the S. atlantis-hesperis complex. We then used ecological models to predict habitat suitability for each of the three recovered genomic lineages in the S. atlantis-hesperis complex and assessed their pairwise niche divergence. These analyses resolved that these three lineages are significantly diverged in their respective niches and are not separated by discontinuities in suitable habitat that might present barriers to gene flow. We therefore infer that ecologically-mediated selection resulting in disparate habitat associations is a principal mechanism reinforcing their genomic integrity. Overall, our results unambiguously support significant evolutionary and ecological divergence between the northern and southern lineages of S. hesperis, sufficient to recognize the southern evolutionary lineage as a distinct species, called S. nausicaa based on taxonomic priority.

Species Delimitation Under Allopatry: Genomic Divergences Within and Across Continents in Lepidoptera

“…The copyright holder for this preprint this version posted March 7, 2023. ; https://doi.org/10.1101/2023.03.06.531242 doi: bioRxiv preprint single entities is often false as these populations frequently show strong intra-continental substructuring (D'Ercole et al 2021;Campbell et al 2022).…”

“…Consequently, we refrain to make any formal taxonomic actions here. For example, our underlying assumption of the uniformity of the North American populations as single entities is often false as these populations frequently show strong intra-continental sub- structuring (D’Ercole et al 2021; Campbell et al 2022).…”

“…single entities is often false as these populations frequently show strong intra-continental substructuring(D'Ercole et al 2021;Campbell et al 2022). …”

Genomic evidence for contrasting patterns of host‐associated genetic differentiation across shared host‐plant species in leaf‐ and bud‐galling sawflies

“…In leaf gallers, however, we instead found clear frequency differences across Salix host species but an absence of strict reciprocal monophyly, a pattern resembling the barcode‐based results of Leppänen et al (2014). Mitonuclear discordance following from incomplete lineage sorting or hybridization is common in insects (e.g., Campbell et al, 2022; Linnen & Farrell, 2007; Lopez‐Vaamonde et al, 2021), and the haplodiploid sex determination system of sawflies and other hymenopterans biases introgression towards mitochondria (Patten et al, 2015; Prous et al, 2020). Porous species boundaries are a probable explanation for the genetic composition of bud galler BG050 in our data set: the specimen was reared from S. myrsinifolia and was grouped within the E. myrsinifoliae clade in the mtDNA tree, but appears to represent a case of mixed ancestry based on SNP data (Figure 3).…”

Genome-wide markers show continental structuring and mitonuclear discordance in the forest tent caterpillar (Malacosoma disstria Hübner) (Lepidoptera: Lasiocampidae)

“…However, due to its reduced effective population size and unique pattern of maternal inheritance, this single genetic region can be shaped by neutral or selective forces that do not influence other (i.e., nuclear) genetic markers (Funk and Omland 2003;Ballard and Whitlock 2004;Rubinoff et al 2006). Hence, the evolutionary history of the mitochondrial genome may not reflect the overall history of a species and may provide limited or contradictory information relative to the nuclear genome for interand intraspecific genomic variation, leading to observations of mitonuclear discordance (Roe and Sperling 2007;Galtier et al 2009;Dupuis et al 2012;Toews and Brelsford 2012;Teske et al 2018;Campbell et al 2022). Detecting discordance between the mitochondrial and nuclear genomes requires a complementary approach, with both mitochondrial and nuclear markers sampled from the same individuals.…”