Genetic Basis of Body Color and Spotting Pattern in Redheaded Pine Sawfly Larvae (<i>Neodiprion lecontei</i>)

Linnen, Catherine R.; O'Quin, Claire Tamplain; Shackleford, Taylor; Sears, Connor R.; Lindstedt, Carita

doi:10.1534/genetics.118.300793

Cited by 26 publications

(32 citation statements)

References 110 publications

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“…Although numerous studies have focused on the genetic basis of adaptive pigmentation in insects (e.g., Nadeau et al 2016; Yassin et al 2016; Linnen et al 2018), color variation in these systems plays diverse ecological roles and Biston remains as the clearest example of cryptic background matching (Cook and Saccheri 2013). By contrast, in vertebrate systems, there are a growing number of studies investigating the genetic basis of crypsis.…”

Section: Introductionmentioning

confidence: 99%

The population genetics of crypsis in vertebrates: recent insights from mice, hares, and lizards

et al. 2019

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By combining well-established population genetic theory with high-throughput sequencing data from natural populations, major strides have recently been made in understanding how, why, and when vertebrate populations evolve crypsis. Here, we focus on background matching, a particular facet of crypsis that involves the ability of an organism to conceal itself through matching its color to the surrounding environment. While interesting in and of itself, the study of this phenotype has also provided fruitful population genetic insights into the interplay of strong positive selection with other evolutionary processes. Specifically, and predicated upon the findings of previous candidate gene association studies, a primary focus of this recent literature involves the realization that the inference of selection from DNA sequence data first requires a robust model of population demography in order to identify genomic regions which do not conform to neutral expectations. Moreover, these demographic estimates provide crucial information about the origin and timing of the onset of selective pressures associated with, for example, the colonization of a novel environment. Furthermore, such inference has revealed crypsis to be a particularly useful phenotype for investigating the interplay of migration and selection-with examples of gene flow constraining rates of adaptation, or alternatively providing the genetic variants that may ultimately sweep through the population. Here, we evaluate the underlying evidence, review the strengths and weaknesses of the many population genetic methodologies used in these studies, and discuss how these insights have aided our general understanding of the evolutionary process.

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Section: Introductionmentioning

confidence: 99%

The population genetics of crypsis in vertebrates: recent insights from mice, hares, and lizards

et al. 2019

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“…Interspecific variation in clutch size may also arise if the relationship between clutch size and larval survival varies among species. For example, some Neodiprion species have aposematic coloration (Tostwaryk 1972; Linnen et al 2018). When aposematic signals are used, group-living can enhance the efficacy of those signals (Gamberale and Tullberg 1998; Hatle and Salazar 2001; Riipi et al 2001).…”

Section: Discussionmentioning

confidence: 99%

Mother knows best: maternal egg-clutch size predicts larval group size in pine sawflies (genusNeodiprion)

2019

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Evolutionary conflicts are pervasive in nature and have the potential to drive antagonistic coevolution of conflict-related traits. However, when such conflicts are weak or idiosyncratic, phenotypic signatures of coevolutionary arms races may be absent. Here, we ask whether variation in group-living traits among pine-sawfly species in the genus Neodiprion is consistent with a history of parent-offspring conflict. To address this question, we compile data on adult female clutch size, larval aggregation behavior, and larval group size for a monophyletic group of 19 eastern North American Neodiprion species from field observations, laboratory assays, and published descriptions. We then evaluate the extent to which each trait exhibits phylogenetic signal and, based on these results, examine correlations between group-size traits both with and without phylogenetic correction. Although female oviposition behavior and larval grouping behavior varies among species and variation in these traits is decoupled from phylogeny, we find no evidence of antagonistic coevolution between these traits. Furthermore, while larvae are physically capable of dispersal, female clutch size is a strong predictor of larval colony size, indicating that larvae do not substantially alter initial group size after hatching. Thus, although theoretical work demonstrates the potential for parent-offspring conflict over group size in animals that lack parental care, our data suggest that this type of conflict is not likely to be a long-term driver of phenotypic evolution.

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“…Based on the ecology of N. lecontei (Figure 1), we were specifically looking for genes involved in digestion, detoxification, pigmentation, gregarious behavior, chemosensation, immune function, and reproduction. We first asked whether any of our top differentially expressed genes corresponded to candidate genes in existing manually curated gene datasets for N. lecontei (chemosensation, detoxification, and immunity genes: (Vertacnik et al, in prep); pigmentation genes: (Linnen et al, 2018)). For remaining genes, we identified the closest Drosophila orthologue and used the gene ontology (GO) term database to determine the likely function for each gene.…”

Section: Methodsmentioning

confidence: 99%

“…In addition to the complete metamorphic event that occurs during the pupal stage, there are two metamorphic transitions that occur within the larval stage of the redheaded pine sawfly that result in pronounced changes in coloration and behavior (Atwood & Peck, 1943; Coppel & Benjamin, 1965; Linnen, O’Quin, Shackleford, Sears, & Lindstedt, 2018) and references therein) (Figure 1A). The first metamorphic transition is a shift from a “cryptic” to an “aposematic” feeding larval morph and is less dramatic than the other transitions (hereafter, “minor metamorphosis”).…”

Section: Introductionmentioning

confidence: 99%

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

Herrig

Vertacnik

Kohrs

et al. 2019

Preprint

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Complex life cycles-especially those with distinct larval and adult stages separated by a complete metamorphic event-are common in animals. 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 decoupled (i.e., genetically uncorrelated) 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. Significance Statement8 out of 10 animals undergo a metamorphic transition at some point in their life. The adaptive decoupling hypothesis proposes that metamorphosis is widespread because it enables natural selection to act independently on traits expressed at different stages. Using four ecologically distinct life stages of the redheaded pine sawfly, we show that the dissimilarity of gene expression profiles can be predicted based on the ecological dissimilarity of the life stages and on whether these genes impact ecological interactions. We also find that gene expression is more dissimilar between drastic life stages than between different sexes. Together, these results provide strong support for a core assumption of the ADH: that metamorphosis enables organisms to optimize genetic correlations across development.

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Genetic Basis of Body Color and Spotting Pattern in Redheaded Pine Sawfly Larvae (Neodiprion lecontei)

Cited by 26 publications

References 110 publications

The population genetics of crypsis in vertebrates: recent insights from mice, hares, and lizards

The population genetics of crypsis in vertebrates: recent insights from mice, hares, and lizards

Mother knows best: maternal egg-clutch size predicts larval group size in pine sawflies (genusNeodiprion)

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

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