Abstract
Recent molecular phylogenetic studies of the insect order Lepidoptera have robustly resolved family-level divergences within most superfamilies, and most divergences among the relatively species-poor early-arising superfamilies. In sharp contrast, relationships among the superfamilies of more advanced moths and butterflies that comprise the mega-diverse clade Apoditrysia (ca. 145,000 spp.) remain mostly poorly supported. This uncertainty, in turn, limits our ability to discern the origins, ages and evolutionary consequences of traits hypothesized to promote the spectacular diversification of Apoditrysia. Low support along the apoditrysian “backbone” probably reflects rapid diversification. If so, it may be feasible to strengthen resolution by radically increasing the gene sample, but case studies have been few. We explored the potential of next-generation sequencing to conclusively resolve apoditrysian relationships. We used transcriptome RNA-Seq to generate 1579 putatively orthologous gene sequences across a broad sample of 40 apoditrysians plus four outgroups, to which we added two taxa from previously published data. Phylogenetic analysis of a 46-taxon, 741-gene matrix, resulting from a strict filter that eliminated ortholog groups containing any apparent paralogs, yielded dramatic overall increase in bootstrap support for deeper nodes within Apoditrysia as compared to results from previous and concurrent 19-gene analyses. High support was restricted mainly to the huge subclade Obtectomera broadly defined, in which 11 of 12 nodes subtending multiple superfamilies had bootstrap support of 100%. The strongly supported nodes showed little conflict with groupings from previous studies, and were little affected by changes in taxon sampling, suggesting that they reflect true signal rather than artifacts of massive gene sampling. In contrast, strong support was seen at only 2 of 11 deeper nodes among the “lower”, non-obtectomeran apoditrysians. These represent a much harder phylogenetic problem, for which one path to resolution might include further increase in gene sampling, together with improved orthology assignments.
Highlights
The insect order Lepidoptera is arguably the largest single radiation of plant-feeding insects
The goal of this study was to assess the degree to which RNA-Seq transcriptome data can increase the support for relationships among the superfamilies of Apoditrysia over that found in our previous 19-gene study [22]
If random error is sufficiently reduced by massive gene sampling, strong but misleading bootstrap support might arise from even subtle forms of pervasive systematic error, such as minor compositional heterogeneity or slight differences in the relative abundance of strongly-conflicting gene tree topologies, as well as from long-branch attraction due to the typically sparse taxon sampling in phylogenomics
Summary
The insect order Lepidoptera (moths and butterflies; >157,000 spp.; [1]) is arguably the largest single radiation of plant-feeding insects. Destructive as agricultural pests, they have become icons for environmental conservation, and supply food and fiber to multiple societies [2]. They provide important model systems for studies of genetics, physiology, development, and many aspects of ecology and evolutionary biology [3], including the question of why herbivorous insects, 25% of earth’s known species, are so species-rich [4,5,6].
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