Biology subjects

Mashoodh, R.

Publications and source records attributed to Mashoodh, R..

10 recordsLinked to original sources

bioRxiv2026

Parental care is a genetic capacitor

Parental care is widespread across the animal kingdom and plays a critical role in offspring development. Yet, its broader genetic and evolutionary impacts remain underexplored. Here, using the biparental burying beetle Nicrophorus vespilloides as a model, we show that parental care acts as a genetic capacitor: it allows genetic variation to accumulate while care is present and releases it when care is disrupted. By experimentally manipulating care, we demonstrate that parental care suppresses genetic variation associated with offspring body size, which is released when care is lost. To investigate the underlying molecular mechanisms, we generate a chromosome-scale genome assembly for N. vespilloides, alongside a single-nucleus gene expression atlas and epigenomic datasets from larvae reared with and without parental care. We find that the loss of parental care induces molecular stress, disrupting the expression of the protein chaperone Hsp83, which is a well-known molecular capacitor, alongside other putative mRNA chaperones. Moreover, our results suggest that parental care buffers development by maintaining an open, responsive chromatin landscape and redundant gene regulatory interactions. Overall, our work reveals that parental care shapes the storage, expression and release of genetic variation with broad implications for adaptation and evolution.

animal behavior and cognition↗

bioRxiv2023

Teaching transposon classification as a means to crowd source the curation of repeat annotation - a tardigrade perspective

The advancement of sequencing technologies results in the rapid release of hundreds of new genome assemblies a year providing unprecedented resources for the study of genome evolution. Within this context, the significance of in-depth analyses of repetitive elements, transposable elements (TEs) in particular, is increasingly recognized in understanding genome evolution. Despite the plethora of available bioinformatic tools for identifying and annotating TEs, the phylogenetic distance of the target species from a curated and classified database of repetitive element sequences constrains any automated annotation effort. Manual curation of raw repeat libraries is deemed essential due to the frequent incompleteness of automatically generated consensus sequences. However, manual curation and classification are time-consuming processes that offer limited short-term academic rewards and are typically confined to a few research groups where methods are taught through hands-on experience. Crowd sourcing efforts could offer a significant opportunity to bridge the gap between learning the methods of curation effectively and empowering the scientific community with high-quality, reusable repeat libraries. Here, we present an example of such crowd sourcing effort developed through both in-person and online courses built around a collaborative peer-reviewed teaching process that can be used as teaching reference guide for similar projects. The collaborative manual curation of TEs from two tardigrade species, for which there were no TE libraries available, resulted in the successful characterization of hundreds of new and diverse TEs: A hidden treasure awaits discovery within non-model organisms.

evolutionary biology↗

bioRxiv2023

Sexual dimorphism in head size in wild burying beetles (Nicrophorus vespilloides)

O_LIMale burying beetles (Nicrophorus vespilloides) carry an additional abdominal segment and produce pheromones but otherwise the species is thought to be sexually monomorphic. Both sexes bear bright orange bands on their black elytra, which probably function as part of a warning display rather than in mate choice. C_LIO_LIAlthough larger individuals are more likely to win contests to secure the small carrion required for reproduction, both sexes compete for this vital breeding resource. In wild populations, the sexes are alike in the mean and distribution in their body size. C_LIO_LIHere we describe a form of sexual size dimorphism in wild populations that has previously been overlooked. We show that males have wider heads than females, for any given body size, and that the scaling relationship with body size is hyperallometric in males, but isometric in females. We also show how absolute head width, and the extent of sexual dimorphism in head width differs among wild populations which are within c.10km of each other. C_LIO_LIWe suggest that head size dimorphism could be adaptive, and could be due to divergent selection arising from task specialisation during biparental care, since the duties of care favoured by males are likely to require a greater bite force. C_LI

evolutionary biology↗

bioRxiv2023

Parental care drives the evolution of molecular genetic variation

Cooperative social behaviours, such as parental care, have long been hypothesized to relax selection leading to the accumulation of genetic variation in populations. Although the idea has been discussed for decades, there has been relatively little experimental work to investigate how social behaviour contributes to genetic variation in populations. Here, we investigate how parental care can shape molecular genetic variation in the subsocial insect Nicrophorus vespilloides. Using whole genome sequencing of populations that had evolved in the presence or absence of parental care for 30 generations, we show that parental care maintains levels of standing genetic variation. In contrast, under a harsh environment without care, strong directional selection caused a reduction in genetic variation. Furthermore, we show that adaptation to the loss of care is associated with genetic divergence between populations at loci related to stress, morphological development and transcriptional regulation. These data reveal how social behaviour is linked to the genetic processes that shape and maintain genetic diversity within populations, and provides rare empirical evidence for an old hypothesis. Lay SummarySocial behaviours, such as parental care, have long been hypothesized to result in the accumulation of genetic variation in populations. Here, we investigate how parental care can shape molecular genetic variation in a species that perform biparental care, Nicrophorus vespilloides. Using genome sequencing of populations that had evolved in the presence or absence of parental care for 30 generations, we show that parental care maintains levels of standing genetic variation. In contrast, under a harsh environment without care, populations lost genetic variation. Furthermore, we show that adaptation to the loss of care is associated with genetic divergence between populations at genes related to stress, morphological development and transcriptional regulation. These data reveal how social behaviour is linked to the genetic processes that shape and maintain genetic diversity within populations.

evolutionary biology↗

bioRxiv2022

Multilevel selection leads to divergent coadaptation of care-giving parents during pre-hatching parental care

The joint actions of animals in partnerships or social groups evolve under both natural selection, from the wider environment, and social selection, imposed by other members of the pair or group. We used experimental evolution to investigate how jointly expressed actions evolve upon exposure to a new environmental challenge. Our work focused on the evolution of carrion nest preparation by pairs of burying beetles Nicrophorus vespilloides, a joint activity undertaken by the pair but typically led by the male. In previous work, we found that carrion nest preparation evolved to be faster in experimental populations without post-hatching care (No Care lines) than with post-hatching care (Full Care lines). Here we investigate how this joint activity evolved. After 15 generations of experimental evolution, we created heterotypic pairs (No Care females with Full Care males, and No Care males with Full Care females) and compared their carrion nest making with homotypic No Care and Full Care pairs. We found that pairs with No Care males prepared the nest more rapidly than pairs with Full Care males, regardless of the females line of origin. This suggests that males led the way by adapting their nest preparation behaviour to the No Care environment first, with females secondarily co-adapting their behaviour to the males behaviour by reducing their nest preparation behaviour. We discuss how social coadaptations within pairs or groups could act as a post-mating barrier to gene flow.

evolutionary biology↗

bioRxiv2022

Parental care allows genetic variation to accumulate by relaxing selection

Benevolent social behaviours, such as parental care, are thought to enable mildly deleterious mutations to persist. We tested this prediction experimentally using the burying beetle Nicrophorus vespilloides, an insect with biparental care. For 20 generations, we allowed replicate experimental burying beetle populations to evolve either with post-hatching care ( Full Care populations) or without it ( No Care populations). We then established new lineages, seeded from these experimental populations, which we inbred to assess their mutation load. Outbred lineages served as controls. We also tested whether the deleterious effects of a greater mutation load could be concealed by parental care by allowing half the lineages to receive post-hatching care, while half did not. We found that inbred lineages from the Full Care populations went extinct more quickly than inbred lineages from the No Care populations - but only when offspring received no post-hatching care. We infer that Full Care lineages carried a greater mutation load, but that the associated deleterious effects on fitness could be overcome if larvae received parental care. We suggest that the increased mutation load caused by parental care increases a populations dependence upon care. This could explain why care is seldom lost once it has evolved.

evolutionary biology↗

bioRxiv2022

The evolutionary demise of a social interaction: social partners differ in the rate at which interacting phenotypes are lost

Phenotypic plasticity enables animals to adjust their behaviour flexibly to their social environment - sometimes through the expression of adaptive traits that have not been exhibited for several generations. We investigated how long social adaptations can usefully persist when they are not routinely expressed, by using experimental evolution to document the loss of social traits associated with the supply and demand of parental care. We allowed populations of burying beetles Nicrophorus vespilloides to evolve in two social environments for 48 generations in the lab. In Full Care populations, traits associated with the supply and demand of parental care were expressed at every generation, whereas in No Care populations we prevented expression of these traits experimentally. We then revived trait expression in the No Care populations at generations 24, 43 and 48 by allowing parents to supply post-hatching care, and compared these social traits with those expressed by the Full Care populations. We found that offspring demands for care decayed in the No Care populations more rapidly than a parents capacity to supply care. Furthermore, male care decayed before female care. We suggest that this reflects differences in the strength of selection for the expression of alternative traits in offspring, males and females, which can enhance fitness when post-hatching care is disrupted. Impact SummarySocial interactions between animals are suggested to be increasingly vulnerable to breakdown in our changing world. Our experiments offer a rare insight into what happens next, by assessing in real time the durability of social behaviours that are no longer routinely expressed. Our results also have implications for conservation captive breeding programmes where compensatory husbandry techniques prevent trait expression and so could inadvertently induce rapid, irreversible trait loss. We investigated how long it took populations to lose the ability to express appropriate social behaviour when they had been prevented from doing so for many generations. We did this by evolving replicate populations of burying beetles Nicrophorus vespilloides in the laboratory for 48 generations. The burying beetle is a common insect that is well-known for caring for its larvae, although larvae can survive in the lab without any care at all. In two populations ("Full Care"), we allowed parents and offspring to interact during the supply of post-hatching care, as usual. In two other populations ("No Care"), parents were removed before offspring hatched and so could not interact socially with their young. Over the course of 48 generations of experimental evolution, we periodically revived social interactions between parents and offspring in the No Care populations. We assessed the extent to which larval begging behaviours, and parental care behaviours, had decayed by comparing their expression with those in the Full Care populations. We found that larval begging behaviour eroded rapidly in No Care populations, and more rapidly than the supply of care by parents. Furthermore, paternal care decayed to a greater extent than maternal care (which was largely unchanged relative to its expression in the Full Care populations). We suggest that these differences could be due to differences in the strength of selection on each family member for alternative traits to enhance fitness.

evolutionary biology↗

bioRxiv2022

Sex-specific effects of chronic paternal stress on offspring development are partially mediated via mothers.

Paternal stress exposure is known to impact the development of stress-related behaviors in offspring. Previous work has highlighted the importance of sperm mediated factors, such as RNAs, in transmitting the effects of parental stress. However, a key unanswered question is whether mothers behavior could drive or modulate the transmission of paternal stress effects on offspring development. Here we investigate how chronic variable stress in Balb/C mice influences the sex-specific development of anxiety- and depression-like neural and behavioral development in offspring. Moreover, we examined how stressed fathers influenced mate maternal investment towards their offspring and how this may modulate the transmission of paternal stress effects on offspring. We show that paternal stress leads to sex-specific effects on offspring behavior. Males that are chronically stressed sire female offspring that show increased anxiety and depression-like behaviors. However, male offspring of stressed fathers show reductions in anxiety- and depression-behaviors and are generally more exploratory. Moreover, we show that females mated with stressed males gain less weight during pregnancy and provide less care towards their offspring which additionally influenced offspring development. These data indicate that paternal stress can influence offspring development directly and indirectly via changes in mothers, with implications for divergent development between male and female offspring.

neuroscience↗

bioRxiv2021

Evolved changes in DNA methylation in response to the sustained loss of parental care in the burying beetle

Levels of parental care critically influence the developmental environment with the capacity to impact the growth, survival, physiology, and behaviour of offspring. Plastic changes in DNA methylation have been hypothesised to modulate gene expression responses to parental environments. Moreover, these effects can be inherited and so may affect the process of adaptive evolution. In this study, using experimental evolution, we investigated how plastic changes in DNA methylation induced by the loss of parental care have evolved in a biparental insect (Nicrophorus vespilloides) using experimental evolution. We show that removal of care in a single generation is associated with changes in gene expression in stress-related pathways in 1st instar larvae. However, in larvae that have adapted to the loss of parental care after being deprived of care for 30 generations, gene expression is shifted from stress-related gene expression towards growth and brain development pathways. We found that changes in gene body methylation arose both as a direct response to the loss of parental care and stochastically as populations diverged. Overall, our results suggest that a complex interplay between transcription and DNA methylation shapes the molecular adaptation to environmental change.

evolutionary biology↗

bioRxiv2021

Subnuclear localisation is associated with gene activation not repression or parental origin at the imprinted Dlk1-Dio3 locus

At interphase, de-condensed chromosomes have a non-random three-dimensional architecture within the nucleus, however, little is known about the extent to which nuclear organisation might influence expression or vice versa. Here, using imprinting as a model, we use 3D RNA- and DNA-fluorescence-in-situ-hybridisation in normal and mutant mouse embryonic stem cells to assess the relationship between imprinting control, gene expression and allelic distance from the nuclear periphery. We compared the two parentally inherited imprinted domains at the Dlk1-Dio3 domain and find a small but reproducible trend for the maternally inherited domain to be further away from the periphery if the maternally expressed gene Gtl2/Meg3 is active compared to when it is silenced. Using Zfp57KO ES cells, which harbour a paternal to maternal epigenotype switch, we observe active alleles significantly further away from the nuclear periphery with the distance from the periphery being proportional to the number of alleles active within the cell. This distribution of alleles suggests an activating effect of the nuclear interior rather than a repressive association with the nuclear periphery. Although we see a trend for the paternally inherited copy of the locus to be closer to the nuclear periphery, this appears to be linked to stochastic gene expression differences rather than parental origin. Our results suggest that transcriptional activity, rather than transcriptional repression or parental origin, defines sub-nuclear localisation at an endogenous imprinted domain. Author summaryGenomic imprinting is an epigenetically regulated process that results in the preferential expression of a subset of developmentally regulated genes from maternally or paternally inherited chromosomes. We have used imprinted genes as a model system to investigate the relationship between the localisation of genes within the cell nucleus and their active expression while at the same time distinguishing gene repression by genomic imprinting, and gene repression by other mechanisms that act on the active allele. We find that there is a significant correlation between transcription and distance to the edge of the nucleus for the Gtl2/Meg3 gene in the imprinted Dlk1-Dio3 region. However, this correlation has a very small effect size and the nuclear envelope, which is commonly thought to act as a repressive environment for gene expression, does not appear to play a major role. We show that position effects, which have been shown for artificially lamina-targeted genes, also exist for endogenous loci and consider the possible biological relevance of the observed small effect.

molecular biology↗