Publications by authors named "Laura C Lavine"

14 Publications

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Epithelial folding determines the final shape of beetle horns.

Curr Opin Genet Dev 2021 Apr 10;69:122-128. Epub 2021 Apr 10.

Department of Entomology, Washington State University, Pullman, WA, 99163 USA. Electronic address:

The elaborate ornaments and weapons of sexual selection, such as the vast array of horns observed in scarab beetles, are some of the most striking outcomes of evolution. How these novel traits have arisen, develop, and respond to condition is governed by a complex suite of interactions that require coordination between the environment, whole-animal signals, cell-cell signals, and within-cell signals. Endocrine factors, developmental patterning genes, and sex-specific gene expression have been shown to regulate beetle horn size, shape, and location, yet no overarching mechanism of horn shape has been described. Recent advances in microscopy and computational analyses combined with a functional genetic approach have revealed that patterning genes combined with intricate epithelial folding and movement are responsible for the final shape of a beetle head horn.
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http://dx.doi.org/10.1016/j.gde.2021.03.003DOI Listing
April 2021

RNA interference of NADPH-cytochrome P450 reductase increases susceptibilities to multiple acaricides in Tetranychus urticae.

Pestic Biochem Physiol 2020 May 28;165:104550. Epub 2020 Feb 28.

Department of Entomology, Pennsylvania State University, University Park, PA 16802, USA. Electronic address:

The two-spotted spider mite, Tetranychus urticae, is a polyphagous pest feeding on over 1100 plant species, including numerous highly valued economic crops. The control of T. urticae largely depends on the use of acaricides, which leads to pervasive development of acaricide resistance. Cytochrome P450-mediated metabolic detoxification is one of the major mechanisms of acaricide resistance in T. urticae. NADPH-cytochrome P450 reductase (CPR) plays as a crucial co-factor protein that donates electron(s) to microsomal cytochrome P450s to complete their catalytic cycle. This study seeks to understand the involvement of CPR/P450 in acaricide resistance in T. urticae. The full-length cDNA sequence of T. urticae's CPR (TuCPR) was cloned and characterized. TuCPR was ubiquitously transcribed in different life stages of T. urticae and the highest transcription was observed in the nymph and adult stages. TuCPR was constitutively over-expressed in six acaricide resistant populations compared to a susceptible one. TuCPR transcriptional expression was also induced by multiple acaricides in a time-dependent manner. Down-regulation of TuCPR via RNA interference (RNAi) in T. urticae led to reduced enzymatic activities of TuCPR and cytochrome P450s, as well as a reduction of resistance to multiple acaricides, abamectin, bifenthrin, and fenpyroximate. The outcome of this study highlights CPR as a potential novel target for eco-friendly control of T. urticae and other related plant-feeding pests.
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http://dx.doi.org/10.1016/j.pestbp.2020.02.016DOI Listing
May 2020

Multiple insecticide resistance in onion thrips populations from Western USA.

Pestic Biochem Physiol 2020 May 4;165:104553. Epub 2020 Mar 4.

Department of Entomology, Pennsylvania State University, University Park, PA 16802, USA. Electronic address:

Thrips tabaci is a key pest of onions, especially in the Pacific Northwestern USA. Management of T. tabaci is dominated by the application of various insecticides. However, T. tabaci is known to develop insecticide resistance which possibly leads to control failures, crop loss, and environmental concern. Here, we evaluated resistance status of T. tabaci populations from conventional and organic commercial onion fields to three widely used insecticides: oxamyl, methomyl, and abamectin with on-field concentration-mortality bioassays. The biochemistry and molecular mechanisms underlying resistance to these insecticides were also investigated by using enzymatic assays and detecting resistance-associated mutations. Field-evolved resistance to oxamyl, methomyl and abamectin were detected in most of the T. tabaci populations collected from conventional onion farms. At the labeled field rate, all the tested insecticides, particularly methomyl and oxamyl, had significantly reduced efficacy. Enzymatic assays of insecticide target and detoxification enzymes indicated that T. tabaci populations in Western USA onions harbor multiple mechanisms of resistance including enhanced activities of detoxification enzymes and target site insensitivity. Our results provide new information in understanding the dynamics of T. tabaci adaptation to multiple insecticides, which will help to design sustainable insecticide resistance management strategies for T. tabaci. Furthermore, this study provides the foundation for future research in identifying the biochemical and molecular markers associated with insecticide resistance in T. tabaci.
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http://dx.doi.org/10.1016/j.pestbp.2020.104553DOI Listing
May 2020

Physiological resistance alters behavioral response of Tetranychus urticae to acaricides.

Sci Rep 2019 12 17;9(1):19308. Epub 2019 Dec 17.

Irrigated Agriculture Research and Extension Center, Washington State University, Prosser, WA, 99350, USA.

Multiple acaricide resistance in Tetranychus urticae continues to threaten crop production globally, justifying the need to adequately study resistance for sustainable pest management. Most studies on acaricide resistance have focused on the acute contact toxicity of acaricides with little or no information on the behavioral responses elicited after acaricide exposure. Furthermore, the impact of physiological resistance on these behavioral responses remains unknown in most pest species, including T. urticae. We tested the effect of acaricide resistance on contact toxicity, irritancy and repellency of mitochondrial electron transport inhibitor of complex I (MET-I) and mite growth inhibitor (MGI) acaricides on multiple T. urticae strains. We also tested whether acaricides with similar physiological target site/mode of action also elicit similar behavioral effects on T. urticae strains. MET-I acaricides (fenazaquin, fenpyroximate, and pyrabiden) and MGIs (clofentezine, hexythiazox and etoxazole) elicited a dose-dependent irritant and repellent effect on T. urticae. Selection of strains for physiological resistance to these acaricides affected the behavioral response of T. urticae, especially in MET-I resistant strains, that showed reduced irritancy and repellency to MET-I acaricides. Behavioral response also affected the oviposition of T. urticae, where strains generally showed preferential oviposition away from the acaricides. The outcome of this study highlights negative consequences of acaricide resistance that can potentially affect T. urticae management.
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http://dx.doi.org/10.1038/s41598-019-55708-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6917710PMC
December 2019

Sexual dimorphism and heightened conditional expression in a sexually selected weapon in the Asian rhinoceros beetle.

Mol Ecol 2018 12 17;27(24):5049-5072. Epub 2018 Dec 17.

Department of Biology, McMaster University, Hamilton, Ontario, Canada.

Among the most dramatic examples of sexual selection are the weapons used in battles between rival males over access to females. As with ornaments of female choice, the most "exaggerated" sexually selected weapons vary from male to male more widely than other body parts (hypervariability), and their growth tends to be more sensitive to nutritional state or physiological condition compared with growth of other body parts ("heightened" conditional expression). Here, we use RNAseq analysis to build on recent work exploring these mechanisms in the exaggerated weapons of beetles, by examining patterns of differential gene expression in exaggerated (head and thorax horns) and non-exaggerated (wings, genitalia) traits in the Asian rhinoceros beetle, Trypoxylus dichotomus. Our results suggest that sexually dimorphic expression of weaponry involves large-scale changes in gene expression, relative to other traits, while nutrition-driven changes in gene expression in these same weapons are less pronounced. However, although fewer genes overall were differentially expressed in high- vs. low-nutrition individuals, the number of differentially expressed genes varied predictably according to a trait's degree of condition dependence (head horn > thorax horn > wings > genitalia). Finally, we observed a high degree of similarity in direction of effects (vectors) for subsets of differentially expressed genes across both sexually dimorphic and nutritionally responsive growth. Our results are consistent with a common set of mechanisms governing sexual size dimorphism and condition dependence.
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http://dx.doi.org/10.1111/mec.14907DOI Listing
December 2018

The function of appendage patterning genes in mandible development of the sexually dimorphic stag beetle.

Dev Biol 2017 02 16;422(1):24-32. Epub 2016 Dec 16.

Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan.

One of the defining features of the evolutionary success of insects is the morphological diversification of their appendages, especially mouthparts. Although most insects share a common mouthpart ground plan, there is remarkable diversity in the relative size and shapes of these appendages among different insect lineages. One of the most prominent examples of mouthpart modification can be found in the enlargement of mandibles in stag beetles (Coleoptera, Insecta). In order to understand the proximate mechanisms of mouthpart modification, we investigated the function of appendage-patterning genes in mandibular enlargement during extreme growth of the sexually dimorphic mandibles of the stag beetle Cyclommatus metallifer. Based on knowledge from Drosophila and Tribolium studies, we focused on seven appendage patterning genes (Distal-less (Dll), aristaless (al), dachshund (dac), homothorax (hth), Epidermal growth factor receptor (Egfr), escargot (esg), and Keren (Krn). In order to characterize the developmental function of these genes, we performed functional analyses by using RNA interference (RNAi). Importantly, we found that RNAi knockdown of dac resulted in a significant mandible size reduction in males but not in female mandibles. In addition to reducing the size of mandibles, dac knockdown also resulted in a loss of the serrate teeth structures on the mandibles of males and females. We found that al and hth play a significant role during morphogenesis of the large male-specific inner mandibular tooth. On the other hand, knockdown of the distal selector gene Dll did not affect mandible development, supporting the hypothesis that mandibles likely do not contain the distal-most region of the ancestral appendage and therefore co-option of Dll expression is unlikely to be involved in mandible enlargement in stag beetles. In addition to mandible development, we explored possible roles of these genes in controlling the divergent antennal morphology of Coleoptera.
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http://dx.doi.org/10.1016/j.ydbio.2016.12.011DOI Listing
February 2017

Identification and functional analyses of sex determination genes in the sexually dimorphic stag beetle Cyclommatus metallifer.

BMC Genomics 2016 Mar 22;17:250. Epub 2016 Mar 22.

Department of Entomology, Washington State University, Pullman, WA, 99164, USA.

Background: Genes in the sex determination pathway are important regulators of sexually dimorphic animal traits, including the elaborate and exaggerated male ornaments and weapons of sexual selection. In this study, we identified and functionally analyzed members of the sex determination gene family in the golden metallic stag beetle Cyclommatus metallifer, which exhibits extreme differences in mandible size between males and females.

Results: We constructed a C. metallifer transcriptomic database from larval and prepupal developmental stages and tissues of both males and females. Using Roche 454 pyrosequencing, we generated a de novo assembled database from a total of 1,223,516 raw reads, which resulted in 14,565 isotigs (putative transcript isoforms) contained in 10,794 isogroups (putative identified genes). We queried this database for C. metallifer conserved sex determination genes and identified 14 candidate sex determination pathway genes. We then characterized the roles of several of these genes in development of extreme sexual dimorphic traits in this species. We performed molecular expression analyses with RT-PCR and functional analyses using RNAi on three C. metallifer candidate genes--Sex-lethal (CmSxl), transformer-2 (Cmtra2), and intersex (Cmix). No differences in expression pattern were found between the sexes for any of these three genes. In the RNAi gene-knockdown experiments, we found that only the Cmix had any effect on sexually dimorphic morphology, and these mimicked the effects of Cmdsx knockdown in females. Knockdown of CmSxl had no measurable effects on stag beetle phenotype, while knockdown of Cmtra2 resulted in complete lethality at the prepupal period. These results indicate that the roles of CmSxl and Cmtra2 in the sex determination cascade are likely to have diverged in stag beetles when compared to Drosophila. Our results also suggest that Cmix has a conserved role in this pathway. In addition to those three genes, we also performed a more complete functional analysis of the C. metallifer dsx gene (Cmdsx) to identify the isoforms that regulate dimorphism more fully using exon-specific RNAi. We identified a total of 16 alternative splice variants of the Cmdsx gene that code for up to 14 separate exons. Despite the variation in RNA splice products of the Cmdsx gene, only four protein isoforms are predicted. The results of our exon-specific RNAi indicated that the essential CmDsx isoform for postembryonic male differentiation is CmDsxB, whereas postembryonic female specific differentiation is mainly regulated by CmDsxD.

Conclusions: Taken together, our results highlight the importance of studying the function of highly conserved sex determination pathways in numerous insect species, especially those with dramatic and exaggerated sexual dimorphism, because conservation in protein structure does not always translate into conservation in downstream function.
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http://dx.doi.org/10.1186/s12864-016-2522-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4802893PMC
March 2016

Molecular mechanisms of Tetranychus urticae chemical adaptation in hop fields.

Sci Rep 2015 Dec 1;5:17090. Epub 2015 Dec 1.

Irrigated Agriculture Research and Extension Center, Washington State University, Prosser, WA 99350, USA.

The two-spotted spider mite, Tetranychus urticae Koch is a major pest that feeds on >1,100 plant species. Many perennial crops including hop (Humulus lupulus) are routinely plagued by T. urticae infestations. Hop is a specialty crop in Pacific Northwest states, where 99% of all U.S. hops are produced. To suppress T. urticae, growers often apply various acaricides. Unfortunately T. urticae has been documented to quickly develop resistance to these acaricides which directly cause control failures. Here, we investigated resistance ratios and distribution of multiple resistance-associated mutations in field collected T. urticae samples compared with a susceptible population. Our research revealed that a mutation in the cytochrome b gene (G126S) in 35% tested T. urticae populations and a mutation in the voltage-gated sodium channel gene (F1538I) in 66.7% populations may contribute resistance to bifenazate and bifenthrin, respectively. No mutations were detected in Glutamate-gated chloride channel subunits tested, suggesting target site insensitivity may not be important in our hop T. urticae resistance to abamectin. However, P450-mediated detoxification was observed and is a putative mechanism for abamectin resistance. Molecular mechanisms of T. urticae chemical adaptation in hopyards is imperative new information that will help growers develop effective and sustainable management strategies.
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http://dx.doi.org/10.1038/srep17090DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4664861PMC
December 2015

Functional mechanics of beetle mandibles: Honest signaling in a sexually selected system.

J Exp Zool A Ecol Genet Physiol 2016 Jan 9;325(1):3-12. Epub 2015 Sep 9.

Department of Biology, Gonzaga University, Spokane, Washington.

Male stag beetles possess colossal mandibles, which they wield in combat to obtain access to females. As with many other sexually selected weapons, males with longer mandibles win more fights. However, variation in the functional morphology of these structures, used in male-male combat, is less well understood. In this study, mandible bite force, gape, structural strength, and potential tradeoffs are examined across a wide size range for one species of stag beetle, Cyclommatus metallifer. We found that not only does male mandible size demonstrate steep positive allometry, but the shape, relative bite force, relative gape, and safety factor of the mandibles also change with male size. Allometry in these functionally important mandibular traits suggests that larger males with larger mandibles should be better fighters, and that the mandibles can be considered an honest signal of male fighting ability. However, negative allometry in mandible structural safety factor, wing size, and flight muscle mass suggest significant costs and a possible limit on the size of the mandibles. J. Exp. Zool. 325A:3-12, 2016. © 2015 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/jez.1961DOI Listing
January 2016

The Fat/Hippo signaling pathway links within-disc morphogen patterning to whole-animal signals during phenotypically plastic growth in insects.

Dev Dyn 2015 Sep 14;244(9):1039-1045. Epub 2015 Jul 14.

Department of Entomology, Washington State University, Pullman, Washington.

Background: Insects exhibit a diversity of environmentally sensitive phenotypes that allow them to be an extraordinarily successful group. For example, mandible size in male stag beetles is exquisitely sensitive to the larval nutritional environment and is a reliable signal of male condition.

Results: To date, studies of how such phenotypically plastic traits develop have focused on two types of mechanistic processes. Local, tissue-specific genetic mechanisms specify the shape and approximate final size of structures, whereas whole-animal hormonal signaling mechanisms modulate trait growth in response to environmental circumstance, including the body size and nutritional state of each individual. Hormones such as juvenile hormone, ecdysteroids, and/or ligands of the insulin-signaling pathway specify whether traits grow and regulate how much growth occurs across a diversity of insect groups. What remains to be shown is how the local, tissue-specific developmental genetic pathways interact with these whole animal hormonal signaling pathways during development to yield phenotypically plastic patterns of trait growth.

Conclusions: Because the Fat/Hippo signaling pathway coordinates trait growth and development through its interactions with morphogens and hormonal pathways, we propose that Fat/Hippo signaling is a missing mechanistic link coordinating environmentally sensitive trait development in insects. Developmental Dynamics 244:1039-1045, 2015. © 2015 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/dvdy.24296DOI Listing
September 2015

Is diversification in male reproductive traits driven by evolutionary trade-offs between weapons and nuptial gifts?

Proc Biol Sci 2015 May;282(1807):20150247

Department of Entomology, China Agricultural University, Beijing 100193, China

Many male animals have evolved exaggerated traits that they use in combat with rival males to gain access to females and secure their reproductive success. But some male animals invest in nuptial gifts that gains them access to females. Both these reproductive strategies are costly in that resources are needed to produce the weapon or nuptial gift. In closely related species where both weapons and nuptial gifts are present, little is known about the potential evolutionary trade-off faced by males that have these traits. In this study, we use dobsonflies (order Megaloptera, family Corydalidae, subfamily Corydalinae) to examine the presence and absence of enlarged male weapons versus nuptial gifts within and among species. Many dobsonfly species are sexually dimorphic, and males possess extremely enlarged mandibles that they use in battles, whereas in other species, males produce large nuptial gifts that increase female fecundity. In our study, we show that male accessory gland size strongly correlates with nuptial gift size and that when male weapons are large, nuptial gifts are small and vice versa. We mapped weapons and nuptial gifts onto a phylogeny we constructed of 57 species of dobsonflies. Our among-species comparison shows that large nuptial gift production evolved in many species of dobsonfly but is absent from those with exaggerated weapons. This pattern supports the potential explanation that the trade-off in resource allocation between weapons and nuptial gifts is important in driving the diversity of male mating strategies seen in the dobsonflies, whereas reduced male-male competition in the species producing large spermatophores could be an alternative explanation on their loss of male weapons. Our results shed new light on the evolutionary interplay of multiple sexually selected traits in animals.
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http://dx.doi.org/10.1098/rspb.2015.0247DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4424648PMC
May 2015

Insights into the development and evolution of exaggerated traits using de novo transcriptomes of two species of horned scarab beetles.

PLoS One 2014 20;9(2):e88364. Epub 2014 Feb 20.

Department of Entomology, Washington State University, Pullman, Washington, United States of America.

Scarab beetles exhibit an astonishing variety of rigid exo-skeletal outgrowths, known as "horns". These traits are often sexually dimorphic and vary dramatically across species in size, shape, location, and allometry with body size. In many species, the horn exhibits disproportionate growth resulting in an exaggerated allometric relationship with body size, as compared to other traits, such as wings, that grow proportionately with body size. Depending on the species, the smallest males either do not produce a horn at all, or they produce a disproportionately small horn for their body size. While the diversity of horn shapes and their behavioural ecology have been reasonably well studied, we know far less about the proximate mechanisms that regulate horn growth. Thus, using 454 pyrosequencing, we generated transcriptome profiles, during horn growth and development, in two different scarab beetle species: the Asian rhinoceros beetle, Trypoxylus dichotomus, and the dung beetle, Onthophagus nigriventris. We obtained over half a million reads for each species that were assembled into over 6,000 and 16,000 contigs respectively. We combined these data with previously published studies to look for signatures of molecular evolution. We found a small subset of genes with horn-biased expression showing evidence for recent positive selection, as is expected with sexual selection on horn size. We also found evidence of relaxed selection present in genes that demonstrated biased expression between horned and horn-less morphs, consistent with the theory of developmental decoupling of phenotypically plastic traits.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0088364PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3930525PMC
January 2015

Developmental link between sex and nutrition; doublesex regulates sex-specific mandible growth via juvenile hormone signaling in stag beetles.

PLoS Genet 2014 Jan 16;10(1):e1004098. Epub 2014 Jan 16.

Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido, Japan.

Sexual dimorphisms in trait expression are widespread among animals and are especially pronounced in ornaments and weapons of sexual selection, which can attain exaggerated sizes. Expression of exaggerated traits is usually male-specific and nutrition sensitive. Consequently, the developmental mechanisms generating sexually dimorphic growth and nutrition-dependent phenotypic plasticity are each likely to regulate the expression of extreme structures. Yet we know little about how either of these mechanisms work, much less how they might interact with each other. We investigated the developmental mechanisms of sex-specific mandible growth in the stag beetle Cyclommatus metallifer, focusing on doublesex gene function and its interaction with juvenile hormone (JH) signaling. doublesex genes encode transcription factors that orchestrate male and female specific trait development, and JH acts as a mediator between nutrition and mandible growth. We found that the Cmdsx gene regulates sex differentiation in the stag beetle. Knockdown of Cmdsx by RNA-interference in both males and females produced intersex phenotypes, indicating a role for Cmdsx in sex-specific trait growth. By combining knockdown of Cmdsx with JH treatment, we showed that female-specific splice variants of Cmdsx contribute to the insensitivity of female mandibles to JH: knockdown of Cmdsx reversed this pattern, so that mandibles in knockdown females were stimulated to grow by JH treatment. In contrast, mandibles in knockdown males retained some sensitivity to JH, though mandibles in these individuals did not attain the full sizes of wild type males. We suggest that moderate JH sensitivity of mandibular cells may be the default developmental state for both sexes, with sex-specific Dsx protein decreasing sensitivity in females, and increasing it in males. This study is the first to demonstrate a causal link between the sex determination and JH signaling pathways, which clearly interact to determine the developmental fates and final sizes of nutrition-dependent secondary-sexual characters.
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http://dx.doi.org/10.1371/journal.pgen.1004098DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3894178PMC
January 2014

A general mechanism for conditional expression of exaggerated sexually-selected traits.

Bioessays 2013 Oct 12;35(10):889-99. Epub 2013 Jul 12.

School of Biological Sciences, University of Bristol, UK.

Sexually-selected exaggerated traits tend to be unusually reliable signals of individual condition, as their expression tends to be more sensitive to nutritional history and physiological circumstance than that of other phenotypes. As such, these traits are the foundation for many models of sexual selection and animal communication, such as "handicap" and "good genes" models. Exactly how expression of these traits is linked to the bearer's condition has been a central yet unresolved question, in part because the underlying physiological mechanisms regulating their development have remained largely unknown. Recent discoveries across animals as diverse as deer, beetles, and flies now implicate the widely conserved insulin-like signaling pathway, as a common physiological mechanism regulating condition-sensitive structures with extreme growth. This raises the exciting possibility that one highly conserved pathway may underlie the evolution of trait exaggeration in a multitude of sexually-selected signal traits across the animal kingdom.
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http://dx.doi.org/10.1002/bies.201300031DOI Listing
October 2013