Ecological correlates of gene family size: the draft genome of the redheaded pine sawfly Neodiprion lecontei

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.

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

Though seemingly bizarre, the dramatic post-embryonic transformation that occurs during metamorphosis is one of the most widespread and successful developmental strategies on the planet. The adaptive decoupling hypothesis (ADH) proposes that metamorphosis is an adaptation for optimizing expression of traits across life stages that experience opposing selection pressures. Similarly, sex-biased expression of traits is thought to evolve in response to sexually antagonistic selection. Both hypotheses predict that traits will be genetically decoupled among developmental stages and sexes, but direct comparisons between stage-specific and sex-specific decoupling are rare. Additionally, tests of the ADH have been hampered by a lack of suitable traits for among-stage comparisons and by uncertainties regarding how much decoupling is to be expected. To fill these voids, we characterize transcriptome-wide patterns of gene-expression decoupling in the hypermetamorphic and sexually dimorphic insect, Neodiprion lecontei. This species has three ecologically and morphologically distinct larval stages separated by molts, as well as a complete metamorphic transition that produces dimorphic adult males and females. Consistent with the ADH, we observe that: (1) the decoupling of gene expression becomes more pronounced as the ecological demands of developmental stages become more dissimilar and (2) gene-expression traits that mediate changing ecological interactions show stronger and more variable decoupling than expression traits that are likely to experience more uniform selection. We also find that gene-expression decoupling is more pronounced among major life stages than between the sexes. Overall, our results demonstrate that patterns of gene-expression decoupling can be predicted based on gene function and organismal ecology.

Genetic basis of body color and spotting pattern in redheaded pine sawfly larvae (Neodiprion lecontei)

ABSTRACTPigmentation has emerged as a premier model for understanding the genetic basis of phenotypic evolution, and a growing catalog of color loci is starting to reveal biases in the mutations, genes, and genetic architectures underlying color variation in the wild. However, existing studies have sampled a limited subset of taxa, color traits, and developmental stages. To expand our sample of color loci, we performed quantitative trait locus (QTL) mapping analyses on two types of larval pigmentation traits that vary among populations of the redheaded pine sawfly (Neodiprion lecontei): carotenoid-based yellow body color and melanin-based spotting pattern. For both traits, our QTL models explained a substantial proportion of phenotypic variation and suggested a genetic architecture that is neither monogenic nor highly polygenic. Additionally, we used our linkage map to anchor the current N. lecontei genome assembly. With these data, we identified promising candidate genes underlying: (1) a loss of yellow pigmentation in Mid-Atlantic/northeastern populations (Cameo2 and apoLTP-II/I), and (2) a pronounced reduction in black spotting in Great-Lakes populations (yellow, TH, Dat). Several of these genes also contribute to color variation in other wild and domesticated taxa. Overall, our findings are consistent with the hypothesis that predictable genes of large-effect contribute to color evolution in nature.

Sequence and Organization of the Neodiprion lecontei Nucleopolyhedrovirus Genome

ABSTRACT All fully sequenced baculovirus genomes, with the exception of the dipteran Culex nigripalpus nucleopolyhedrovirus (CuniNPV), have previously been from Lepidoptera. This study reports the sequencing and characterization of a hymenopteran baculovirus, Neodiprion lecontei nucleopolyhedrovirus (NeleNPV), from the redheaded pine sawfly. NeleNPV has the smallest genome so far published (81,755 bp) and has a GC content of only 33.3%. It contains 89 potential open reading frames, 43 with baculovirus homologues, 6 identified by conserved domains, and 1 with homology to a densovirus structural protein. Average amino acid identity of homologues ranged from 19.7% with CuniNPV to 24.9% with Spodoptera exigua nucleopolyhedrovirus. The conserved set of baculovirus genes has dropped to 29, since NeleNPV lacks an F protein homologue (ac23/ld130). NeleNPV contains 12 conserved lepidopteran baculovirus genes, including that for DNA binding protein, late expression factor 11 (lef-11), polyhedrin, occlusion derived virus envelope protein-18 (odv-e18), p40, and p45, but lacks 21 others, including lef-3, me53, immediate early gene-1, lef-6, pp31, odv-e66, few polyhedra 25k, odv-e25, protein kinase-1, fibroblast growth factor, and ubiquitin. The lack of identified baculovirus homologues may be due to difficulties in identification, differences in host-virus interactions, or other genes performing similar functions. Gene parity plots showed limited colinearity of NeleNPV with other baculoviruses, and phylogenetic analysis indicates that NeleNPV may have existed before the lepidopteran nucleopolyhedrovirus and granulovirus divergence. The creation of two new Baculoviridae genera to fit hymenopteran and dipteran baculoviruses may be necessary.

Influence of elevated CO2, nitrogen, and Pinus elliottii genotypes on performance of the redheaded pine sawfly, Neodiprion lecontei

Slash pine (Pinus elliottii Engelm. var. elliottii) seedlings were grown in open-top chambers receiving ambient or elevated atmospheric CO2 (~365 or ~720 µL·L–1). Seedlings received low or high soil nitrogen treatments (0.02 or 0.2 mg N·g–1) and represented three families varying in resistance to fusiform rust (Cronartium quercuum (Berk.) Miyabe ex Shirai f. sp. fusiforme (Hedgc. & N. Hunt) Burdsall & G. Snow). Following 18 months of exposure to treatment conditions, current-year needles were fed to larvae of the redheaded pine sawfly (Neodiprion lecontei (Fitch)). Needle N concentration and water content were lower in elevated-CO2 and in low-N treatments. Total phenolics increased under high-CO2 and low-N conditions and were highest in the resistant family. Condensed tannins did not vary on the basis of CO2 or N but were higher in needles from the resistant family. Alterations in needle chemistry were associated with variations in sawfly growth and development. Larvae performed most poorly on the family most resistant to fusiform rust, suggesting that the mechanism for resistance was similar in both cases. Relative consumption rates increased with CO2-enriched needle diets but were depressed for resistant needles, suggesting deterrence from the higher total phenolics in this family. Diets using CO2-enriched needles or resistant needles or needles from low-N fertilization treatments resulted in lower relative growth rates for the larvae. Days to pupation increased for larvae fed CO2-enriched and low-N needles. These results suggest that the redheaded pine sawfly could suffer as the level of atmospheric CO2 continues to rise.