scholarly journals Evolutionary Proteomics Reveals Distinct Patterns of Complexity and Divergence between Lepidopteran Sperm Morphs

2019 ◽  
Vol 11 (7) ◽  
pp. 1838-1846 ◽  
Author(s):  
Emma Whittington ◽  
Timothy L Karr ◽  
Andrew J Mongue ◽  
Steve Dorus ◽  
James R Walters

Abstract Spermatozoa are one of the most strikingly diverse animal cell types. One poorly understood example of this diversity is sperm heteromorphism, where males produce multiple distinct morphs of sperm in a single ejaculate. Typically, only one morph is capable of fertilization and the function of the nonfertilizing morph, called parasperm, remains to be elucidated. Sperm heteromorphism has multiple independent origins, including Lepidoptera (moths and butterflies), where males produce a fertilizing eupyrene sperm and an apyrene parasperm, which lacks a nucleus and nuclear DNA. Here we report a comparative proteomic analysis of eupyrene and apyrene sperm between two distantly related lepidopteran species, the monarch butterfly (Danaus plexippus) and Carolina sphinx moth (Manduca sexta). In both species, we identified ∼700 sperm proteins, with half present in both morphs and the majority of the remainder observed only in eupyrene sperm. Apyrene sperm thus have a distinctly less complex proteome. Gene ontology (GO) analysis revealed proteins shared between morphs tend to be associated with canonical sperm cell structures (e.g., flagellum) and metabolism (e.g., ATP production). GO terms for morph-specific proteins broadly reflect known structural differences, but also suggest a role for apyrene sperm in modulating female neurobiology. Comparative analysis indicates that proteins shared between morphs are most conserved between species as components of sperm, whereas morph-specific proteins turn over more quickly, especially in apyrene sperm. The rapid divergence of apyrene sperm content is consistent with a relaxation of selective constraints associated with fertilization and karyogamy. On the other hand, parasperm generally exhibit greater evolutionary lability, and our observations may therefore reflect adaptive responses to shifting regimes of sexual selection.

2018 ◽  
Author(s):  
Emma Whittington ◽  
Tim Karr ◽  
Andrew J. Mongue ◽  
Steve Dorus ◽  
James R. Walters

AbstractSpermatozoa are one of the most strikingly diverse animal cell types. One poorly understood example of this diversity is sperm heteromorphism, where males produce multiple distinct morphs of sperm in a single ejaculate. Typically, only one morph is capable of fertilization and the function of the non-fertilizing morph, called parasperm, remains to be elucidated. Sperm heteromorphism has multiple independent origins, including Lepidoptera (moths and butterflies), where males produce a fertilizing eupyrene sperm and an apyrene parasperm, which lacks a nucleus and nuclear DNA. Here we report a comparative proteomic analysis of eupyrene and apyrene sperm between two distantly related lepidopteran species, the monarch butterfly (Danausplexippus) and Carolina sphinx month (Manduca sexta). In both species, we identified approximatey 700 sperm proteins, with half present in both morphs and the majority of the remainder specific to eupyrene sperm. Apyrene sperm thus have a distinctly less complex proteome. Gene Ontology (GO) analysis revealed proteins shared between morphs tend to be associated with canonical sperm cell structures (e.g. flagellum) and metabolism (e.g. ATP production). GO terms for morph-specific proteins broadly reflect known structural differences, but also suggest a role for apyrene sperm in modulating female neurobiology. Comparative analysis indicates that proteins shared between morphs are most conserved between species as components of sperm, while morph-specific proteins turn over more quickly, especially in apyrene sperm. The rapid divergence of apyrene sperm content is consistent with a relaxation of selective constraints associated with fertilization and karyogamy. On the other hand, parasperm exhibit greater evolutionary lability, which may reflect adaptive response to shifting regimes of sexual selection. Additionally, we provide the first (to our knowledge) scanning electron micrographs of lepidopteran sperm.


2019 ◽  
Vol 116 (8) ◽  
pp. 3006-3011 ◽  
Author(s):  
J. H. Boyle ◽  
H. J. Dalgleish ◽  
J. R. Puzey

Monarch butterfly (Danaus plexippus) decline over the past 25 years has received considerable public and scientific attention, in large part because its decline, and that of its milkweed (Asclepias spp.) host plant, have been linked to genetically modified (GM) crops and associated herbicide use. Here, we use museum and herbaria specimens to extend our knowledge of the dynamics of both monarchs and milkweeds in the United States to more than a century, from 1900 to 2016. We show that both monarchs and milkweeds increased during the early 20th century and that recent declines are actually part of a much longer-term decline in both monarchs and milkweed beginning around 1950. Herbicide-resistant crops, therefore, are clearly not the only culprit and, likely, not even the primary culprit: Not only did monarch and milkweed declines begin decades before GM crops were introduced, but other variables, particularly a decline in the number of farms, predict common milkweed trends more strongly over the period studied here.


2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Lori Peacock ◽  
Chris Kay ◽  
Chloe Farren ◽  
Mick Bailey ◽  
Mark Carrington ◽  
...  

AbstractMeiosis is a core feature of eukaryotes that occurs in all major groups, including the early diverging excavates. In this group, meiosis and production of haploid gametes have been described in the pathogenic protist, Trypanosoma brucei, and mating occurs in the salivary glands of the insect vector, the tsetse fly. Here, we searched for intermediate meiotic stages among trypanosomes from tsetse salivary glands. Many different cell types were recovered, including trypanosomes in Meiosis I and gametes. Significantly, we found trypanosomes containing three nuclei with a 1:2:1 ratio of DNA contents. Some of these cells were undergoing cytokinesis, yielding a mononucleate gamete and a binucleate cell with a nuclear DNA content ratio of 1:2. This cell subsequently produced three more gametes in two further rounds of division. Expression of the cell fusion protein HAP2 (GCS1) was not confined to gametes, but also extended to meiotic intermediates. We propose a model whereby the two nuclei resulting from Meiosis I undergo asynchronous Meiosis II divisions with sequential production of haploid gametes.


Insects ◽  
2021 ◽  
Vol 12 (6) ◽  
pp. 567
Author(s):  
Misty Stevenson ◽  
Kalynn L. Hudman ◽  
Alyx Scott ◽  
Kelsey Contreras ◽  
Jeffrey G. Kopachena

Based on surveys of winter roost sites, the eastern migratory population of the monarch butterfly (Danaus plexippus) in North America appears to have declined in the last 20 years and this has prompted the implementation of numerous conservation strategies. However, there is little information on the survivorship of first-generation monarchs in the core area of occupancy in Texas, Oklahoma, and Louisiana where overwinter population recovery begins. The purpose of this study was to determine the survivorship of first-generation eggs to third instars at a site in north Texas and to evaluate host plant arthropods for their effect on survivorship. Survivorship to third instar averaged 13.4% and varied from 11.7% to 15.6% over three years. The host plants harbored 77 arthropod taxa, including 27 predatory taxa. Despite their abundance, neither predator abundance nor predator richness predicted monarch survival. However, host plants upon which monarchs survived often harbored higher numbers of non-predatory arthropod taxa and more individuals of non-predatory taxa. These results suggest that ecological processes may have buffered the effects of predators and improved monarch survival in our study. The creation of diverse functional arthropod communities should be considered for effective monarch conservation, particularly in southern latitudes.


Author(s):  
George B. Stefano ◽  
Richard M. Kream

AbstractMitochondrial DNA (mtDNA) heteroplasmy is the dynamically determined co-expression of wild type (WT) inherited polymorphisms and collective time-dependent somatic mutations within individual mtDNA genomes. The temporal expression and distribution of cell-specific and tissue-specific mtDNA heteroplasmy in healthy individuals may be functionally associated with intracellular mitochondrial signaling pathways and nuclear DNA gene expression. The maintenance of endogenously regulated tissue-specific copy numbers of heteroplasmic mtDNA may represent a sensitive biomarker of homeostasis of mitochondrial dynamics, metabolic integrity, and immune competence. Myeloid cells, monocytes, macrophages, and antigen-presenting dendritic cells undergo programmed changes in mitochondrial metabolism according to innate and adaptive immunological processes. In the central nervous system (CNS), the polarization of activated microglial cells is dependent on strategically programmed changes in mitochondrial function. Therefore, variations in heteroplasmic mtDNA copy numbers may have functional consequences in metabolically competent mitochondria in innate and adaptive immune processes involving the CNS. Recently, altered mitochondrial function has been demonstrated in the progression of coronavirus disease 2019 (COVID-19) due to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection. Accordingly, our review is organized to present convergent lines of empirical evidence that potentially link expression of mtDNA heteroplasmy by functionally interactive CNS cell types to the extent and severity of acute and chronic post-COVID-19 neurological disorders.


2017 ◽  
Vol 46 (3) ◽  
pp. 626-632 ◽  
Author(s):  
Jamie L. Rafter ◽  
Justin F. Vendettuoli ◽  
Liahna Gonda-King ◽  
Daniel Niesen ◽  
Navindra P. Seeram ◽  
...  

Abstract Prey have evolved a number of defenses against predation, and predators have developed means of countering these protective measures. Although caterpillars of the monarch butterfly,Danaus plexippus L., are defended by cardenolides sequestered from their host plants, the Chinese mantidTenodera sinensis Saussure guts the caterpillar before consuming the rest of the body. We hypothesized that this gutting behavior might be driven by the heterogeneous quality of prey tissue with respect to toxicity and/or nutrients. We conducted behavioral trials in which mantids were offered cardenolide-containing and cardenolide-freeD. plexippus caterpillars and butterflies. In addition, we fed mantids starved and unstarvedD. plexippus caterpillars from each cardenolide treatment and nontoxicOstrinia nubilalis Hübner caterpillars. These trials were coupled with elemental analysis of the gut and body tissues of bothD. plexippus caterpillars and corn borers. Cardenolides did not affect mantid behavior: mantids gutted both cardenolide-containing and cardenolide-free caterpillars. In contrast, mantids consumed bothO. nubilalis and starvedD. plexippus caterpillars entirely.Danaus plexippus body tissue has a lower C:N ratio than their gut contents, whileO. nubilalis have similar ratios; gutting may reflect the mantid’s ability to regulate nutrient uptake. Our results suggest that post-capture prey processing by mantids is likely driven by a sophisticated assessment of resource quality.


1979 ◽  
Vol 81 (1) ◽  
pp. 123-136 ◽  
Author(s):  
N Agabian ◽  
M Evinger ◽  
G Parker

An essential event in developmental processes is the introduction of asymmetry into an otherwise undifferentiated cell population. Cell division in Caulobacter is asymmetric; the progeny cells are structurally different and follow different sequences of development, thus providing a useful model system for the study of differentiation. Because the progeny cells are different from one another, there must be a segregation of morphogenetic and informational components at some time in the cell cycle. We have examined the pattern of specific protein segregation between Caulobacter stalked and swarmer daughter cells, with the rationale that such a progeny analysis would identify both structurally and developmentally important proteins. To complement the study, we have also examined the pattern of protein synthesis during synchronous growth and in various cellular fractions. We show here, for the first time, that the association of proteins with a specific cell type may result not only from their periodicity of synthesis, but also from their pattern of distribution at the time of cell division. Several membrane-associated and soluble proteins are segregated asymmetrically between progeny stalked and swarmer cells. The data further show that a subclass of soluble proteins becomes associated with the membrane of the progeny stalked cells. Therefore, although the principal differentiated cell types possess different synthetic capabilities and characteristic proteins, the asymmetry between progeny stalked and swarmer cells is generated primarily by the preferential association of specific soluble proteins with the membrane of only one daughter cell. The majority of the proteins which exhibit this segregation behavior are synthesized during the entire cell cycle and exhibit relatively long, functional messenger RNA half-lives.


2021 ◽  
Vol 118 (16) ◽  
pp. e2024463118
Author(s):  
Anurag A. Agrawal ◽  
Katalin Böröczky ◽  
Meena Haribal ◽  
Amy P. Hastings ◽  
Ronald A. White ◽  
...  

For highly specialized insect herbivores, plant chemical defenses are often co-opted as cues for oviposition and sequestration. In such interactions, can plants evolve novel defenses, pushing herbivores to trade off benefits of specialization with costs of coping with toxins? We tested how variation in milkweed toxins (cardenolides) impacted monarch butterfly (Danaus plexippus) growth, sequestration, and oviposition when consuming tropical milkweed (Asclepias curassavica), one of two critical host plants worldwide. The most abundant leaf toxin, highly apolar and thiazolidine ring–containing voruscharin, accounted for 40% of leaf cardenolides, negatively predicted caterpillar growth, and was not sequestered. Using whole plants and purified voruscharin, we show that monarch caterpillars convert voruscharin to calotropin and calactin in vivo, imposing a burden on growth. As shown by in vitro experiments, this conversion is facilitated by temperature and alkaline pH. We next employed toxin-target site experiments with isolated cardenolides and the monarch’s neural Na+/K+-ATPase, revealing that voruscharin is highly inhibitory compared with several standards and sequestered cardenolides. The monarch’s typical >50-fold enhanced resistance to cardenolides compared with sensitive animals was absent for voruscharin, suggesting highly specific plant defense. Finally, oviposition was greatest on intermediate cardenolide plants, supporting the notion of a trade-off between benefits and costs of sequestration for this highly specialized herbivore. There is apparently ample opportunity for continued coevolution between monarchs and milkweeds, although the diffuse nature of the interaction, due to migration and interaction with multiple milkweeds, may limit the ability of monarchs to counteradapt.


2012 ◽  
Vol 12 (2) ◽  
pp. 204-214 ◽  
Author(s):  
Christopher P. Stefan ◽  
Nannan Zhang ◽  
Takaaki Sokabe ◽  
Alberto Rivetta ◽  
Clifford L. Slayman ◽  
...  

ABSTRACT In the budding yeast Saccharomyces cerevisiae , mating pheromones activate a high-affinity Ca 2+ influx system (HACS) that activates calcineurin and is essential for cell survival. Here we identify extracellular K + and a homologous pair of transmembrane proteins, Kch1 and Kch2 (Prm6), as necessary components of the HACS activation mechanism. Expression of Kch1 and especially Kch2 was strongly induced during the response to mating pheromones. When forcibly overexpressed, Kch1 and Kch2 localized to the plasma membrane and activated HACS in a fashion that depended on extracellular K + but not pheromones. They also promoted growth of trk1 trk2 mutant cells in low K + environments, suggesting they promote K + uptake. Voltage-clamp recordings of protoplasts revealed diminished inward K + currents in kch1 kch2 double-mutant cells relative to the wild type. Conversely, heterologous expression of Kch1 in HEK293T cells caused the appearance of inwardly rectifying K + currents. Collectively, these findings suggest that Kch1 and Kch2 directly promote K + influx and that HACS may electrochemically respond to K + influx in much the same way as the homologous voltage-gated Ca 2+ channels in most animal cell types.


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