Genome assembly and methylome analysis of the white wax scale insect provides insight into sexual differentiation of metamorphosis in hexapods

Scale insects are hemimetabolous, showing “incomplete” metamorphosis and no true pupal stage. Ericerus pela, commonly known as the white wax scale insect (hereafter, WWS), is a wax-producing insect found in Asia and Europe. WWS displays dramatic sexual dimorphism, with notably different metamorphic fates in males and females. Males develop into winged adults, while females are neotenic and maintain a nymph-like appearance, which are flightless and remain stationary. Here we report the de novo assembly of the WWS genome with its size of 638.30 Mb (69.68Mb for scaffold N50) by PacBio sequencing and Hi-C. From these data, we constructed a robust phylogenetic analysis of 24,923 gene families from 16 representative insect genomes, which indicates that holometabola evolved from incomplete metamorphosis insects in the Late Carboniferous, about 50 million years earlier than previously thought. To study the distinct development of males and females, we analyzed the methylome landscape in either sex. Surprisingly, WWS displayed high levels of methylation (4.42% for males) when compared to other insects. We observed differential methylation patterns for genes involved in steroid and sesquiterpenoids production as well as related fatty acid metabolism pathways. We show here that both males and females exhibit distinct titer profiles for ecdysone, the principal insect steroid hormone, and juvenile hormone (a sesquiterpenoid), suggesting that these hormones are the primary drivers of sexually dimorphic features. Our results provide a comprehensive genomic and epigenomic resource of scale insects that provide new insights into the evolution of metamorphosis and sexual dimorphism in insects.

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First Case of Dual Size Asymmetry in an Identical Arthropod Organ: Different Asymmetries of the Combative (Sexual) and Cutting (Non-Sexual) Parts of Mandibles in the Horned Stored-Product Beetle Gnatocerus cornutus (Fabricius, 1798)

Insects ◽

10.3390/insects9040151 ◽

2018 ◽

Vol 9 (4) ◽

pp. 151 ◽

Cited By ~ 1

Author(s):

Tomas Vendl ◽

Vaclav Stejskal ◽

Radek Aulicky

Keyword(s):

Sexual Dimorphism ◽

Regulatory Mechanisms ◽

Directional Asymmetry ◽

Sexually Dimorphic ◽

First Case ◽

Males And Females ◽

Long Life ◽

High Degree ◽

Size Asymmetry ◽

Single Organ

Although it is known that separate insect body structures may be asymmetrical within one species, the different functional asymmetries within a single organ as a result of differential selective regimes have not been described. Based on microscopic measurements and SEM photography, we examined the size, shape and asymmetry of the mandibular structures of males and females of the sexually dimorphic broad-horned flour beetle, Gnatocerus cornutus (Tenebrionidae, Coleoptera). It was found that sexual dimorphism only manifests in certain outgrowth parts (horns) of male mandibles, while the remaining cutting parts of the mandibles hold identical morphologies for both sexes. A more interesting finding—since this is the first published case of dual functionally selected asymmetry in an identical arthropod organ—was that the cutting part of the male mandible exhibited directional asymmetry, whereas the outgrowth horn part of the mandible showed a high degree of symmetry. Moreover, there was no relationship between the size and asymmetry of horns. The results indicate different regulatory mechanisms of sexually selected combative horns and the food-functional, more conservative (constrained by hard food and adult long life) cutting parts of mandibles.

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Differences in Pelvic Fin Length Represent Sexual Dimorphism in Utah Chub (Gila atraria)

The Open Fish Science Journal ◽

10.2174/1874401x01407010042 ◽

2014 ◽

Vol 7 (1) ◽

pp. 42-45 ◽

Cited By ~ 1

Author(s):

Mark C. Belk ◽

Scott Bird ◽

Mehmet Cemal Oguz ◽

Jerald B. Johnson

Keyword(s):

Body Size ◽

Sexual Dimorphism ◽

Cyprinid Fish ◽

Sexually Dimorphic ◽

Adaptive Function ◽

Males And Females ◽

The Difference ◽

Sexually Mature ◽

Fin Length ◽

Pelvic Fin

The cyprinid fish Gila atraria Girard (Utah chub) is generally considered a sexually monomorphic species. However, prior observations revealed variation in pelvic fin length within populations that appears sexually dimorphic. We measured the relative pelvic fin length of 419 sexually mature Utah chub from 8 different locations to determine the magnitude and generality of this apparent dimorphism. Pelvic fin length in G. atraria differs between sexes by about 10% on average; males have longer pelvic fins than females. The dimorphism is general across all locations, but it is not related to body size. Magnitude of the dimorphism varies by predation environment – the difference between males and females is slightly greater in low predation environments. We find no evidence for an adaptive function for this dimorphism; however, it does provide an efficient mechanism for determining sex without dissection.

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Hydraulic constraints of reproduction do not explain sexual dimorphism in the genus Leucadendron (Proteaceae)

10.1101/209460 ◽

2017 ◽

Author(s):

Adam B. Roddy ◽

Justin van Blerk ◽

Jeremy J. Midgley ◽

Adam G. West

Keyword(s):

Sexual Dimorphism ◽

Fire Frequency ◽

Sexually Dimorphic ◽

Hydraulic Efficiency ◽

Costs Of Reproduction ◽

Dioecious Species ◽

Shoot Architecture ◽

Males And Females ◽

And Function ◽

In Fire

AbstractBecause of the importance of reproduction in plant life history, the physiological costs of reproduction often influence vegetative structure and function. In dioecious species, these effects can be quite obvious, as different costs of male and female reproductive functions are entirely separated among different individuals in a population. In fire-prone ecosystems, in which recruitment is driven by fire frequency, many plants will maintain their seeds in the canopy, only to be released after a fire. The dioecious genus Leucadendron is a notable case of this, as females can maintain their seed cones for years, and, even more interestingly, species in the genus differ substantially in the degree to which males and females are sexually dimorphic. A recent study (Harris and Pannell 2010) argued that the hydraulic costs of maintaining seed cones for many years would effect the degree of sexual dimorphism among species. However, this assumed that shoot hydraulic architecture would be related to traits exhibiting sexual dimorphism. Here we explicitly test this hypothesis on two Leucadendron species. We found (1) that metrics of branch ramification used in the previous study to characterize dimorphism do not conform to known scaling relationships and (2) that sexual dimorphism in shoot architecture has no effect on hydraulic efficiency. Both of these results seriously question the pattern described by Harris and Pannell (2010) and suggest that the hydraulic costs of prolonged seed retention in Leucadendron do not significantly affect branch architecture.

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Genome sequence of the Chinese white wax scale insect Ericerus pela: the first draft genome for the Coccidae family of scale insects

GigaScience ◽

10.1093/gigascience/giz113 ◽

2019 ◽

Vol 8 (9) ◽

Cited By ~ 1

Author(s):

Pu Yang ◽

Shuhui Yu ◽

Junjun Hao ◽

Wei Liu ◽

Zunling Zhao ◽

...

Keyword(s):

Genome Sequence ◽

Draft Genome ◽

Gene Families ◽

Sister Group ◽

Scale Insect ◽

Fatty Acyl ◽

Scale Insects ◽

Sequence Length ◽

Evolutionary Analysis ◽

Chinese White

AbstractBackgroundThe Chinese white wax scale insect, Ericerus pela, is best known for producing wax, which has been widely used in candle production, casting, Chinese medicine, and wax printing products for thousands of years. The secretion of wax, and other unusual features of scale insects, is thought to be an adaptation to their change from an ancestral ground-dwelling lifestyle to a sedentary lifestyle on the higher parts of plants. As well as helping to improve its economic value, studies of E. pela might also help to explain the adaptation of scale insects. However, no genomic data are currently available for E. pela.FindingsTo assemble the E. pela genome, 303.92 Gb of data were generated using Illumina and Pacific Biosciences sequencing, producing 277.22 Gb of clean data for assembly. The assembled genome size was 0.66 Gb, with 1,979 scaffolds and a scaffold N50 of 735 kb. The guanine + cytosine content was 33.80%. A total of 12,022 protein-coding genes were predicted, with a mean coding sequence length of 1,370 bp. Twenty-six fatty acyl-CoA reductase genes and 35 acyltransferase genes were identified. Evolutionary analysis revealed that E. pela and aphids formed a sister group and split ∼241.1 million years ago. There were 214 expanded gene families and 2,219 contracted gene families in E. pela.ConclusionWe present the first genome sequence from the Coccidae family. These results will help to increase our understanding of the evolution of unique features in scale insects, and provide important genetic information for further research.

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The evolution of derived monomorphism from sexual dimorphism: A case study on salamanders

Integrative Organismal Biology ◽

10.1093/iob/obaa044 ◽

2020 ◽

Author(s):

Nancy L Staub

Keyword(s):

Sexual Dimorphism ◽

The Other ◽

Head Width ◽

Social Selection ◽

Sexually Dimorphic ◽

Ecological Significance ◽

Selective Forces ◽

Males And Females ◽

Shed Light

Abstract While sexual dimorphism has long received special attention from biologists, derived monomorphism, the condition in which both males and females express similar derived features, has been less well studied. Historically, the appearance of “male-like” features in females has been explained by the genetic correlation between the sexes. Recent work emphasizes the importance of studying the independent selective forces on both females and males to understand sexual dimorphism. Sexual dimorphism and derived monomorphism in the genus Aneides are examined in light of predictions of social selection. Aneides hardii shows the greatest degree of sexual dimorphism in snout-vent length and head width, with the other species of Aneides less sexually dimorphic. This reduced dimorphism, however, is not a return to an ancestral monomorphic state, but rather exemplifies derived monomorphism because females express traits that were limited in expression to males of ancestral species. Instead of calling these “male-typical” traits in females, I suggest the term “derived monomorphic” traits, as these traits are typical in these females and “derived monomorphic” can apply to both sexes. Increased attention to studying the patterns and ecological significance of derived monomorphism will shed light on the underlying selective forces, including sexual selection, on both females and males.

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High rates of evolution preceded shifts to sex-biased gene expression in Leucadendron, the most sexually dimorphic angiosperms

10.1101/2021.01.12.426328 ◽

2021 ◽

Author(s):

Mathias Scharmann ◽

Anthony G Rebelo ◽

John R Pannell

Keyword(s):

Gene Expression ◽

Sexual Dimorphism ◽

Rapid Evolution ◽

Sex Bias ◽

Sexually Dimorphic ◽

Expression Levels ◽

Rates Of Evolution ◽

Expression Evolution ◽

Males And Females ◽

Species Specific

AbstractThe males and females of many dioecious plants differ in morphological (Dawson and Geber 1999; Barrett and Hough 2013; Tonnabel et al. 2017), physiological (Juvany and Munné-Bosch 2015), life-history (Delph 1999), and defence traits (Cornelissen and Stiling 2005). Ultimately, such sexual dimorphism must largely be due to differential gene expression between the sexes (Ellegren and Parsch 2007), but little is known about how sex-biased genes are recruited and how their expression evolves over time. We measured gene expression in leaves of males and females of ten species sampled across the South African Cape genus Leucadendron, which shows repeated changes in sexual dimorphism and includes the most extreme differences between males and females in flowering plants (Midgley 2010; Barrett and Hough 2013; Tonnabel et al. 2014). Even in the most dimorphic species in our sample, fewer than 2% of genes showed sex-biased gene expression (SBGE) in vegetative tissue, with surprisingly little correspondence between SBGE and vegetative dimorphism across species. The identity of sex-biased genes in Leucadendron was highly species-specific, with a rapid turnover among species. In animals, sex-biased genes often evolve more quickly than unbiased genes in their sequences and expression levels (Ranz et al. 2003; Khaitovich et al. 2005; Ellegren and Parsch 2007; Voolstra et al. 2007; Harrison et al. 2015; Naqvi et al. 2019), consistent with hypotheses invoking rapid evolution due to sexual selection. Our phylogenetic analysis in Leucadendron, however, clearly indicates that sex-biased genes are recruited from a class of genes with ancestrally rapid rates of expression evolution, perhaps due to low evolutionary or pleiotropic constraints. Nevertheless, we also find evidence for adaptive evolution of expression levels once sex bias evolves. Thus, although the expression of sex-biased genes is ultimately responsive to selection, high rates of expression evolution might usually predate the evolution of sex bias.

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Growth and Sexual Dimorphism in the Dibbler, Parantechinus apicalis (Marsupialia, Dasyuridae)

Australian Mammalogy ◽

10.1071/am00239 ◽

1999 ◽

Vol 21 (2) ◽

pp. 239

Author(s):

H. Mills ◽

Z. German R ◽

C. Lambert ◽

P. Bradley M

Keyword(s):

Sexual Dimorphism ◽

Mating Systems ◽

Growth Patterns ◽

Sexually Dimorphic ◽

Breeding Strategies ◽

Wild Animals ◽

Selective Pressures ◽

Morphological Studies ◽

In Captivity ◽

Males And Females

Sexual dimorphism in animals has been recognised as being associated with particular breeding strategies or mating systems since Darwin's Origin of Species. Frequently, in polygamous situations, females express a variety of attributes to attract males, and males compete with each other for access to females. This produces different selective pressures in each sex, which in tum produces differing morphologies (Leigh 1995). Thus, the emphasis of morphological studies of sexual differences tends to focus on adults and not the growth patterns that generate those differences. Growth patterns in marsupials have been shown to be variable between species (Gemmell and Hendrikz 1993). Previous studies of dasyurid species in captivity concluded that the onset of dimorphism occurs prior to or during weaning (Whitford, Fanning and White 1982; Williams and Williams 1982), but wild animals are not sexually dimorphic until after weaning (Soderquist 1995). These studies have generally examined the growth rates of males and females and the timing of the onset of sexual dimorphism, but little attention has been focussed on how the differences between the sexes are generated.

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Digit ratio in three species of tropidurid lizards

Herpetozoa ◽

10.3897/herpetozoa.34.e59064 ◽

2021 ◽

Vol 34 ◽

pp. 67-70

Author(s):

Kelton Gonçalves Miranda ◽

Marcella Junqueira Goulart ◽

Conrado Barbosa Galdino

Keyword(s):

Sexual Dimorphism ◽

Sex Hormones ◽

Digit Ratio ◽

Sexually Dimorphic ◽

Lizard Species ◽

Finger Length ◽

Digit Ratios ◽

Selective Forces ◽

Males And Females ◽

Interpopulation Variation

Proportions between pairs of digits are linked to fitness in tetrapods and they can be influenced by sex hormones through individuals’ ontogenies. Therefore, in many species, the proportions amongst finger length ratios (referred as digit ratio, i.e. 2D second and 4D fourth digits) can differ between males and females. We investigated whether the three most commonly used forelimb digit ratios are sexually dimorphic in three tropidurid species. In one of the three lizard species, Eurolophosaurus nanuzae, males and females differ for only 2D:4D digit ratio. Otherwise, our results on the studied Tropidurus species conform to previous studies showing no differences in digit ratios between males and females. Hence, it might be the case of local selective forces shaping interpopulation variation in the expression of sexual dimorphism for digit ratio.

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Sexual dimorphism in the Arachnid orders

PeerJ ◽

10.7717/peerj.5751 ◽

2018 ◽

Vol 6 ◽

pp. e5751 ◽

Cited By ~ 7

Author(s):

Callum J. McLean ◽

Russell J. Garwood ◽

Charlotte A. Brassey

Keyword(s):

Sexual Dimorphism ◽

Body Shape ◽

Sexual Size Dimorphism ◽

Future Research ◽

Sexually Dimorphic ◽

Leg Length ◽

Animal Kingdom ◽

Males And Females ◽

Total Body ◽

Insight Into

Sexual differences in size and shape are common across the animal kingdom. The study of sexual dimorphism (SD) can provide insight into the sexual- and natural-selection pressures experienced by males and females in different species. Arachnids are diverse, comprising over 100,000 species, and exhibit some of the more extreme forms of SD in the animal kingdom, with the males and females of some species differing dramatically in body shape and/or size. Despite this, research on arachnid SD has primarily focused on specific clades as opposed to observing traits across arachnid orders, the smallest of which have received comparatively little attention. This review provides an overview of the research to date on the trends and potential evolutionary drivers for SD and sexual size dimorphism (SSD) in individual arachnid orders, and across arachnids as a whole. The most common trends across Arachnida are female-biased SSD in total body size, male-biased SSD in relative leg length and SD in pedipalp length and shape. However, the evolution of sexually dimorphic traits within the group is difficult to elucidate due to uncertainty in arachnid phylogenetic relationships. Based on the dataset we have gathered here, we highlight gaps in our current understanding and suggest areas for future research.

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Sexual dimorphism in the Drosophila metabolome increases throughout development

10.1101/073148 ◽

2016 ◽

Author(s):

FC Ingleby ◽

Edward H Morrow

Keyword(s):

Gene Expression ◽

Sexual Dimorphism ◽

Metabolic Profiling ◽

Evolutionary Biology ◽

General Pattern ◽

Sexually Dimorphic ◽

Transcriptomic Data ◽

Expression Studies ◽

Males And Females ◽

Gene Expression Studies

AbstractThe expression of sexually dimorphic phenotypes from a shared genome between males and females is a longstanding puzzle in evolutionary biology. Increasingly, research has made use of transcriptomic technology to examine the molecular basis of sexual dimorphism through gene expression studies, but even this level of detail misses the metabolic processes that ultimately link gene expression with the whole organism phenotype. We use metabolic profiling in Drosophila melanogaster to complete this missing step, with a view to examining variation in male and female metabolic profiles, or metabolomes, throughout development. We show that the metabolome varies considerably throughout larval, pupal and adult stages. We also find significant sexual dimorphism in the metabolome, although only in pupae and adults, and the extent of dimorphism tends to increase throughout development. We compare this to transcriptomic data from the same population and find that the general pattern of increasing sex differences throughout development is mirrored in RNA expression. We discuss our results in terms of the usefulness of metabolic profiling in linking genotype and phenotype to more fully understand the basis of sexually dimorphic phenotypes.

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