Support for the Adaptive Decoupling Hypothesis from Whole-Transcriptome Profiles of a Hypermetamorphic and Sexually Dimorphic Insect, Neodiprion lecontei

Herrig, Danielle K; Vertacnik, Kim L.; Kohrs, Anna R; Linnen, Catherine R.

doi:10.22541/au.159909006.64508636

Cited by 6 publications

(9 citation statements)

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“…New gene models were added to subsequent TBLASTN searches and this process continued iteratively until new chemoreceptors were no longer found. The gene models were checked against RNAseq reads from tissue-specific transcriptomes (adult antennae, mouthparts, heads, legs, genitalia, and larval heads (Herrig et al 2019)) and against orthologs in the N. pinetum draft genome assembly (NCBI accession GCA_004916985.1).…”

Section: Methodsmentioning

confidence: 99%

Ecological correlates of gene family size in a pine-feeding sawfly genome and across Hymenoptera

Vertacnik

Herrig

Godfrey

et al. 2021

Preprint

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A central goal in evolutionary biology is to determine the predictability of adaptive genetic changes. Despite many documented cases of convergent evolution at individual loci, little is known about the repeatability of gene family expansions and contractions. To address this void, we examined gene family evolution in the redheaded pine sawfly Neodiprion lecontei, a non-eusocial hymenopteran and exemplar of a pine-specialized lineage evolved from angiosperm-feeding ancestors. After assembling and annotating a draft genome, we manually annotated multiple gene families with chemosensory, detoxification, or immunity functions and characterized their genomic distributions and evolutionary history. Our results suggest that expansions of bitter gustatory receptor (GR), clan 3 cytochrome P450 (CYP3), and antimicrobial peptide (AMP) subfamilies may have contributed to pine adaptation. By contrast, there was no evidence of recent gene family contraction via pseudogenization. Next, we compared the number of genes in these same families across insect taxa that vary in diet, dietary specialization, and social behavior. In Hymenoptera, herbivory was associated with large GR and small olfactory receptor (OR) families, eusociality was associated with large OR and small AMP families, and--unlike investigations among more closely related taxa--ecological specialization was not related to gene family size. Overall, our results suggest that gene families that mediate ecological interactions may expand and contract predictably in response to particular selection pressures, however, the ecological drivers and temporal pace of gene gain and loss likely varies considerably across gene families.

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Section: Methodsmentioning

confidence: 99%

Ecological correlates of gene family size in a pine-feeding sawfly genome and across Hymenoptera

Vertacnik

Herrig

Godfrey

et al. 2021

Preprint

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“…Other examples of decoupling in gene expression come from insects (Jacobs, et al 2006; Fellous and Lazzaro 2011; Saenko, et al 2012; Herrig, et al 2020). For instance, in the hymenopteran Neodiprion lecontei , which has multiple life stages separated by increasingly dramatic metamorphic transitions, Herrig et al (2020) found that a progressively greater proportion of genes (up to 31%) were differentially expressed between each successive pair of stages. That observation matched the authors’ predictions that gene expression decoupling would be strongest between the most ecologically dissimilar life stages.…”

Section: Discussionmentioning

confidence: 99%

Genomic and Spectral Visual Adaptation in Southern Leopard Frogs during the Ontogenetic Transition from Aquatic to Terrestrial Light Environments

Schott

Bell

Loew

et al. 2021

Preprint

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Many animals have complex life cycles where larval and adult forms have distinct ecologies and habitats that impose different demands on their sensory systems. While the adaptive decoupling hypothesis predicts reduced genetic correlations between life stages, how sensory systems adapt across life stages at the molecular level is not well understood. Frogs are a compelling system to study this question in because most species rely on vision as both aquatic tadpoles and terrestrial adults, but these habitats present vastly different light environments. Here we used whole eye transcriptome sequencing to investigate differential expression between aquatic tadpoles and terrestrial juveniles of the southern leopard frog (Lithobates sphenocephalus). Because visual physiology changes with light levels, we also tested how constant light or dark exposure affected gene expression. We found 42% of genes were differentially expressed in the eyes of tadpoles versus juveniles, versus 5% for light/dark exposure. Analyses targeting a curated set of visual genes revealed significant differential expression between life stages in genes that control aspects of visual function and development, including spectral sensitivity and lens composition. Light/dark exposure had a significant effect on a smaller set of visual genes. Finally, microspectrophotometry of photoreceptors confirmed shifts in spectral sensitivity predicted by the expression results, consistent with adaptation to distinct light environments. Overall, we identified extensive expression-level differences in the eyes of tadpole and juvenile frogs related to observed morphological and physiological changes through metamorphosis, and corresponding adaptive shifts to optimize vision in aquatic versus terrestrial environments.

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“…Additional work is also needed to evaluate the "effect size" (i.e., how much an allele or trait increases reproductive isolation) of body size relative to other reproductive barriers and other potential magic traits (Servedio et al 2011;Nosil and Schluter 2011). Fortunately, growing genomic resources (Vertacnik et al 2017;Herrig et al 2021) and the ability to rear and cross these species in the lab (Bendall et al 2017) make this a highly tractable system for uncovering the genetic and ecological mechanisms underlying magic traits and speciation.…”

Section: Is Body Size Really "Magic" In Pine Sawflies?mentioning

confidence: 99%

Body size as a magic trait in two plant-feeding insect species

Glover

Bendall

Terbot

et al. 2022

Preprint

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When gene flow accompanies speciation, recombination can decouple divergently selected loci and loci conferring reproductive isolation. This barrier to sympatric divergence disappears when assortative mating and disruptive selection involve the same "magic" trait. Although magic traits could be widespread, the relative importance of different types of magic traits to speciation remains unclear. Because body size frequently contributes to host adaptation and assortative mating in plant-feeding insects, we evaluated several magic trait predictions for this trait in a pair of sympatricNeodiprionsawfly species adapted to different pine hosts. A large morphological dataset revealed that sawfly adults from populations and species that use thicker-needled pines are consistently larger than those that use thinner needled-pines. Fitness data from recombinant backcross females revealed that egg size is under divergent selection between the preferred pines. Lastly, mating assays revealed strong size-assortative mating within and between species in three different crosses, with the strongest prezygotic isolation between populations that have the greatest interspecific size differences. Together, our data support body size as a magic trait in pine sawflies and possibly many other plant-feeding insects. Our work also demonstrates how intraspecific variation in morphology and ecology can cause geographic variation in the strength of prezygotic isolation.

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Support for the Adaptive Decoupling Hypothesis from Whole-Transcriptome Profiles of a Hypermetamorphic and Sexually Dimorphic Insect, Neodiprion lecontei

Cited by 6 publications

References 0 publications

Ecological correlates of gene family size in a pine-feeding sawfly genome and across Hymenoptera

Ecological correlates of gene family size in a pine-feeding sawfly genome and across Hymenoptera

Genomic and Spectral Visual Adaptation in Southern Leopard Frogs during the Ontogenetic Transition from Aquatic to Terrestrial Light Environments

Body size as a magic trait in two plant-feeding insect species

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