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Reinhardt, K.

Publications and source records attributed to Reinhardt, K..

10 recordsLinked to original sources

Drosophila sperm carry a dietary sterol that increases offspring development

Diet affects male fitness directly and across generations. The current research focus is on dietary proteins and carbohydrates. Dietary lipids (DL), which are incorporated into cell membranes and affect signaling, were neglected or analyzed at pathological high-fat diet amounts. How fitness variation arises among males consuming healthy amounts of DL remains unknown, as do the fitness parameters being affected, including paternal effects. Contrasting mammal- vs. plant-derived DL, we measure mating rate, sperm count, sperm and seminal fluid quality, fertility and offspring growth in Drosophila melanogaster. We show that i) mammal-derived DL increased male fitness in isolation and competition, but without changing sperm numbers. ii) We discovered that lipid microcarriers in the seminal fluid fused with, and directly provided DL to sperm, changing sperm quality. iii) Dietary cholesterol, precursor of the growth hormone ecdysone, was incorporated into sperm, vectored to the zygote and improved offspring development and survival. This duality of Drosophila sperm function - fertilization and provision of growth hormone precursor - is an elegant, adaptive solution to prevent rival males from exploiting paternal provision. Direct offspring benefits vectored by sperm offer additional and alternative explanations for the evolution of sperm competition, sperm gigantism, and of anisogamy, the driver of sexual selection.

evolutionary biology↗

Evolution and adaptations of the seminal proteome in an insect with traumatic insemination

The protein composition of sperm and seminal fluid are key to male fitness. However, we currently lack an understanding of the factors that shape seminal proteome composition. The common bedbug (Cimex lectularius) mates by traumatic insemination, subjecting the ejaculate to a unique selective environment as sperm traverse the female genital and paragenital system. We provide the first high-throughput proteomic characterisation of the sperm and seminal fluid proteome in a hemimetabolous insect and the first in-depth proteomic characterisation of the male bedbug reproductive system. Our analysis revealed conserved and unique features of the sperm and seminal fluid proteome with possible links to features of sperm behaviour linked to traumatic insemination. The sperm proteome showed elevated rates of molecular evolution, unlike most other studied species. Conversely, the sperm proteome also contained many conserved proteins. Notably, we found an expansion of Sperm-leucylaminopeptidases (S-Laps) in bedbugs and other hemimetabolous insects, suggesting the origin of S-Laps is perhaps even more ancient than previously thought. Using in silico protein-ligand binding predictions, we show that S-Laps have likely retained catalytic activity. Our results provide a list of candidate proteins involved in reproduction and a foundation for future studies of this expanding global pest.

evolutionary biology↗

Novel female reproductive organ differentiates postmating transcriptional response to insemination versus arrival of sperm in bedbugs

Following the evolution of internal fertilisation, the female reproductive tract became the site of reproductive interactions. However, our understanding of the evolution of female reproductive tract function, including postmating responses critical for reproductive success, are taxonomically limited. Traumatic insemination in the common bedbug (Cimex lectularius) presents an unusual scenario under which postmating responses unfold. Bedbugs have evolved a novel organ, the mesospermalege, that is the site of initial ejaculate x female interactions. As the female reproductive tract does not take receipt of the ejaculate until several hours after mating, bedbugs provide a unique opportunity to explore the evolution of a novel reproductive organ that decouples postmating female responses involved in mating and transfer of the ejaculate from sperm storage, ovulation, and oviposition. Here we show that the mesospermalege has a gene expression profile consistent with functions of ejaculate processing and immune response normally found in the lower reproductive tract of other insect species. In parallel, the postmating response in the lower female reproductive tract is delayed, coinciding with movement of sperm through the female, clearly showing that the postmating response has evolved in response to sperm receipt rather than being an innate function of the tissue. Notably, we also found expression of male seminal fluid genes in the mesospermalege, indicating that intersexual molecular dynamics influence the evolution of reproductive tissues. Our results provide insights into the evolution of novel reproductive traits and female postmating physiology in a global pest with an unusual reproductive biology. SIGNIFICANCEReproduction poses one of the most persistent challenges faced by animals whereby females undergo a series of physiological changes after mating. The independent origin of a reproductive organ in bedbugs (called the mesospermalege) which has evolved to alleviate the costs of traumatic insemination presents a unique case to study the evolution of a novel trait and postmating physiology. Using transcriptomics, we show that many genes normally expressed in the female reproductive tract are instead expressed in the mesospermalege. The reproductive tract also shows a delayed postmating transcriptional response coinciding with sperm entry into the reproductive tract. Our results provide insights into the evolution of reproductive traits and female postmating physiology in a global pest with an unusual reproductive biology.

evolutionary biology↗

Sperm storage reduces sperm and embryo quality in animals

In many animals, sperm are stored for extended periods either in the reproductive tracts of males before ejaculation, or of females after copulation. Sperm storage reduces the risk of sperm limitation in both sexes and avoids the costs of female re-mating. However, sperm storage can lead to post-meiotic sperm senescence, i.e. within-sperm-age-dependent deterioration, potentially impacting conceived offspring and lowering male and female fitness. Yet, the extent and magnitude of such deterioration and the variables modulating it during sperm storage are not well understood. Using a meta-analysis across humans (115 studies) and non-human animals (56 studies from 30 species), we investigate how in-vivo sperm storage affects sperm quality, fertilisation success, and offspring quality. In humans, sperm storage leads to greater sperm oxidative stress and DNA damage, and reduces sperm viability and motility. In other animals, sperm performance and embryo quality decline. We identify the duration of sperm storage, the design used for sampling individuals, and the sex of the individual storing sperm as potentially important moderators of the effects of sperm storage. These findings have key biomedical implications, including optimising the timing of ejaculation and fertilisation in fertility clinics or captive breeding programs. Overall, our results reveal the mechanisms that cause post-meiotic sperm senescence, the fitness consequences of sperm storage, and provide evolutionary insights into sex-specific adaptations that potentially mitigate the detrimental effects of sperm storage.

evolutionary biology↗

Testing for age- and sex- specific mitonuclear epistasis in Drosophila

The need for efficient ATP production is predicted to result in the evolution of cooperation between the mitochondrial and nuclear encoded components of the electron transport system. Novel (i.e., mismatched) mitonuclear genotype combinations are therefore predicted to result in negative fitness consequences, which may become more prevalent with ageing. Such negative fitness effects are expected to be prominent in males, since maternal inheritance of mitochondria is predicted to lead to accumulation of male-harming mutations (the mothers curse hypothesis). To test these predictions, we measured female and male fertility traits using a genetically diverse panel of 27 mitonuclear populations of Drosophila melanogaster with matched or experimentally mismatched mitonuclear genomes at different ages. We found no overall effect of mitonuclear mismatch. In females, we found no effect of mitonuclear epistasis. In males, we found limited evidence of mitonuclear epistasis affecting fitness in old age, however, not in the direction predicted. Experimentally mismatched males sired more offspring in one comparison. Sex-specific advantages of mismatched males might arise if novel nuclear alleles compensate for deleterious mitochondrial alleles that have accumulated. If such compensatory effects of novel mitonuclear combinations increasing fitness occur in nature, they could represent a possible counterforce to the mothers curse.

evolutionary biology↗

The sperm-associated microbiota of crickets and their local variation and rapid turnover

While studying aspects of the sperm biology and immunity of two species of crickets, we encountered bacteria that were released from the male sperm container, the spermatophore, alongside sperm. We describe a presumably rich microbe flora in the sperm population ( sperm-associated microbiota). These sperm-associated microbiota differed between the two species of cricket and between different populations and showed functional diversity. Further, sperm-associated microbiota killed sperm, highlighting their potential role in fitness, especially since they are most likely transferred to females during mating.

evolutionary biology↗

Mito-nuclear variation in transgenerational and reproductive effects of amino acid and lipid nutrition

Epistasis between mitochondrial and nuclear genomes can modulate fitness effects of nutrition. Are these "mitonuclear" effects deterministic with regard to optimal nutrition? Which nutrients and genetic loci participate? Here, in fruitflies, we show that mitonuclear epistasis repeatably dictates fitness effects of dietary lipids and amino acids, with a tripartite interaction emerging as an unprecedented source of quantitative variation. We also observed diet-dependent developmental lethality and parental effects, but only in specific mitonucleotypes. Associating phenotype to mtDNA variation implicated a non-coding RNA (mt:lrRNA), suggesting a novel mechanism, with epistasis between mitochondria-derived regulatory factors and the nuclear genome producing qualitative differences in how diet impacts fitness. SUMMARYCombined action of nuclear genotype and regulatory loci on mtDNA produces major differences in fitness impacts of nutrition.

genetics↗

Interactions between cytoplasmic and nuclear genomes confer sex-specific effects on lifespan in Drosophila melanogaster

A large body of studies has demonstrated that genetic variation that resides outside of the cell nucleus can affect the organismal phenotype. The cytoplasm is home to the mitochondrial genome and, at least in arthropods, often hosts intracellular endosymbiotic bacteria such as Wolbachia. While numerous studies have implicated epistatic interactions between cytoplasmic and nuclear genetic variation as key to mediating patterns of phenotypic expression, two outstanding questions remain. Firstly, the relative contribution of mitochondrial genetic variation to other cytoplasmic sources of variation in shaping the phenotypic outcomes of cyto-nuclear interactions remains unknown. Secondly, it remains unclear whether the outcomes of cyto-nuclear interactions will manifest differently across the two sexes, as might be predicted given that cytoplasmic genomes are screened by natural selection only through females as a consequence of their maternal inheritance. Here, we address these questions, creating a fully-crossed set of replicated cyto-nuclear populations derived from three geographically distinct populations of Drosophila melanogaster, and measuring the lifespan of males and females from each population. We report cyto-nuclear interactions for lifespan, with the outcomes of these interactions differing across the sexes, and reconcile these findings with information on the full mitochondrial sequences and Wolbachia infection status of each of the populations.

evolutionary biology↗

The swim-up technique separates bovine sperm by metabolic rates, motility and tail length

Swim-up is a sperm purification method that is being used daily in andrology labs around the world as a simple step for in vitro sperm selection. This method accumulates the most motile sperm in the upper fraction and leaves sperm with low or no motility in the lower fraction but the underlying reasons are not fully understood. In this article, we compare metabolic rate, motility and sperm tail length of bovine sperm cells of the upper and lower fraction. The metabolic assay platform reveals oxygen consumption rates and extracellular acidification rates simultaneously and thereby delivers the metabolic rates in real time. Our study confirms the upper fraction of bull sperm has improved motility compared to the cells in the lower fraction and shows higher metabolic rates. This pattern was consistent across media of two different levels of viscosity. Sperm with longer flagella are selected in the upper fraction. We conclude that the motility-based separation of the swim-up technique is based on metabolic differences. Metabolic assays could serve as additional or alternative, label-free method to evaluate sperm quality, which is likely particularly useful in cases of asthenozoospermia and teratospermia. Furthermore, metabolic measurements of sperm cells can reveal differences in metabolic pathways in different environments.

zoology↗

A molecular phylogeny of bedbugs elucidates the evolution of host associations and sex-reversal of reproductive trait diversification

All 100+ bedbug species (Cimicidae) are obligate blood-sucking parasites and well-known for their habit of traumatic insemination but the evolutionary trajectory of these characters is unknown. Our new, fossil-dated, molecular phylogeny estimates that ancestral Cimicidae evolved ca. 115MYA as hematophagous specialists on an unidentified host, 50MY before bats, switching to bats and birds thereafter. Humans were independently colonized three times and our phylogeny rejects the idea that the divergence of the two current urban pests (Cimex lectularius and C. hemipterus) 47MYA was associated with the divergence of Homo sapiens and H. erectus (1.6MYA). The females functional reproductive tract is unusually diverse and heterotopic, despite the unusual and strong morphological stasis of the male genitalia. This sex-reversal in genital co-variation is incompatible with current models of genital evolution. The evolutionary trait diversification in cimicids allowed us to uncover fascinating biology and link it to human pre-history and current activity.

ecology↗