The genetics of egg retention and fertilization success in<i>Drosophila</i>: One step closer to understanding the transition from facultative to obligate viviparity

Hórvath, Barbara; Kalinka, Alex T.

doi:10.1111/evo.13411

Cited by 20 publications

(28 citation statements)

References 144 publications

(312 reference statements)

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“…In extreme cases of strong constitutive egg retention, C. elegans strains exhibit partial viviparity, associated with significantly reduced maternal reproduction and survival. Overall, observed genetically variable duration of intra-uterine development in C. elegans thus seems to align well with past reports showing that transitions towards viviparity incur maternal fitness costs as observed for diverse invertebrate and vertebrate taxa with both inter- and intraspecific differences in parity modes (Avise, 2013; Blackburn, 2015; Horváth and Kalinka, 2018; Kalinka, 2015; Ostrovsky et al, 2015; Whittington et al, 2022). To what extent this apparent intergenerational fitness trade-off in C. elegans could involve shaped by parent-offspring conflict (Trivers, 1974) is uncertain.…”

Section: Resultssupporting

confidence: 89%

“…The study of evolutionary transitions between ovi- and viviparity has concentrated on comparisons between species with distinct parity modes, so that evidence is mainly correlative and the genetic changes underlying such transitions can only rarely be determined (Horváth and Kalinka, 2018; Recknagel et al, 2021). Relatively few studies have examined quantitative intraspecific variation in egg retention although this approach may facilitate disentangling its relative costs and benefits.…”

Section: Introductionmentioning

confidence: 99%

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Natural variation in theCaenorhabditis elegansegg-laying circuit modulates an intergenerational fitness trade-off

Mignerot

Gimond

Bolelli

et al. 2023

Preprint

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Evolutionary transitions from oviparity to viviparity are frequent across diverse taxa. Some species also display intraspecific variation in parity mode, or they exhibit an intermediate mode by laying eggs containing embryos at variable, often advanced stages of development. How such natural quantitative variation in egg retention arises through differences in genetics, behaviour, and physiology - and how this variation ultimately connects to variation in specific fitness components - is not well-understood. Here, we study this problem by characterizing intraspecific variation in constitutive retention of fertilized eggs of the nematode Caenorhabditis elegans. Analysing a panel of ~300 wild strains, we find highly variable intra-uterine retention of fertilized eggs, with a fraction of strains showing either strongly reduced or increased egg retention with partial viviparity. We provide evidence for multiple evolutionary origins of such phenotypic extremes and we identify candidate loci explaining this natural variation. Characterizing a subset of wild strains, we confirm that natural variation in egg-laying behaviour contributes to observed differences in egg retention. Using multiple neuromodulatory agents and controlled CRISPR-Cas9-mediated genetic manipulation of endogenous serotonin levels in 10 wild strains, we then show that this behavioural variation arises through an evolutionarily divergent neuromodulatory architecture of the egg-laying circuitry. Intraspecific variation in C. elegans neural circuit activity therefore connects with variation in reproductive strategy, including transitions from oviparity to partial viviparity. In a second objective, we asked why natural variation in C. elegans egg retention might be maintained. Examining potential fitness costs and benefits of this natural variation, we show that strong egg retention reduces maternal fertility and survival, mostly due to detrimental larval hatching in utero. On the other hand, such genotypes with strong egg retention can benefit from improved offspring protection against environmental insults and by gaining a competitive advantage as offspring exhibit a shortened extra-uterine developmental time to reproductive maturity. Observed natural variation in C. elegans egg-laying behaviour may therefore reflect modifications of a trade-off between alternative fitness components expressed across generations. Our study uncovers underappreciated natural diversity in the C. elegans egg-laying circuit and provides insights into the fitness consequences of this behavioural variation. We propose that intraspecific variation in nematode egg-laying behaviour can serve as an ideal system to pinpoint the molecular changes underlying evolutionary transitions between invertebrate ovi- and viviparity.

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Section: Resultssupporting

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Natural variation in theCaenorhabditis elegansegg-laying circuit modulates an intergenerational fitness trade-off

Mignerot

Gimond

Bolelli

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…The resulting effect may be seen in both the laboratory and field oviposition trials as a reduction in oviposition as females are focusing on their own survival rather than egg laying. As eggs are immobile and unable to escape high temperatures, the reduction in reproductive oviposition in August could also be due to the females not depositing eggs in unfavourable environmental conditions and retaining eggs until conditions become optimum [ 40 , 41 ]. Such retention of eggs by D .…”

Section: Discussionmentioning

confidence: 99%

Recording and reproducing the diurnal oviposition rhythms of wild populations of the soft- and stone- fruit pest Drosophila suzukii

Shaw¹,

Fountain²,

Wijnen³

2018

PLoS ONE

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Drosophila suzukii is a horticultural pest on a global scale which causes both yield and economic losses on a range of soft- and stone-fruit. Tackling this pest is problematic but exploiting behavioral rhythms could increase the impact of control. To do this, a better understanding of behavioral patterns is needed. Within this study we aimed to investigate rhythms in reproductive behavior of wild D. suzukii under natural conditions in the field. Environmental parameters were also recorded to decipher how they influence these rhythms. Assays were then performed on laboratory cultures, housed under artificial conditions mimicking the temperature and light cycles, to see if these patterns were reproducible and rhythmic. We were able to promote field like oviposition patterns within the laboratory using realistic temperature and light cycles regardless of variations in other factors including substrate, humidity, and lighting type. Locomotion activity was also recorded under these mimicked conditions to identify how this behavior interacts with oviposition rhythms. Both our field and laboratory assays show that oviposition behavior is likely under the control of the circadian clock and primarily occurs during the day. However, consistent with prior reports we observed that these patterns become crepuscular when day-time temperature peaks exceeded 30°C. This was also found within locomotion rhythms. With an increased understanding of how these behaviors are influenced by environmental conditions, we highlight the importance of using realistic temperature and light cycles when investigating behavioral patterns. From an increased understanding of D. suzukii behavior we increase our ability to target the pest in the field.

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“…As it was observed before (Voigt and Kost 2021), this was more pronounced in females than in males. In response to unfavorable conditions, females sometimes, however, retain their mated eggs (Horváth and Kalinka 2018). Since many PcG targets function in development, and developmental time also varies with temperature (Trotta et al 2006), the observed patterns of temperature-dependent expression could also arise due to females retaining their eggs.…”

Section: Resultsmentioning

confidence: 99%

Genome-wide temperature-sensitivity of PcG regulation and reduction thereof in temperateDrosophila melanogaster

Voigt

Froschauer

2023

Preprint

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Epigenetic regulation varies with the environment. In the fruit fly Drosophila melanogaster, environmental temperature can affect chromatin-based gene regulation. Genes regulated by the Polycomb group (PcG) can vary in their transcriptional output in response to changes in temperature, which typically increases with decreasing temperature. Here, we studied temperature-sensitive expression of PcG target genes on a genome-wide scale, as well as temperature-sensitive enrichment of two histone modifications associated with the regulation of PcG target genes, H3K27me3 and H3K4me3. We investigated temperature-sensitivity in adult flies, and possible differences thereof between populations adapted to temperate and tropical climates. Compared to genes not targeted by the PcG, an elevated number of target genes showed higher expression at the lower temperature, as it is typically observed for PcG regulation. Many of the PcG target genes also exhibited temperature-sensitive H3K4me3 enrichment in the same direction, and the H3K4me3 temperature response correlated positively with that of expression. A small set of target sites also showed temperature-sensitive enrichment of H3K27me3, again with a higher proportion corresponding to increased transcriptional activation at the lower temperature. Overall, higher transcriptional activity at lower temperature was less pronounced in males compared to females, and in temperate compared to tropical flies. Possible trans- and cis-acting factors responsible for reduced expression plasticity in temperate flies were identified, including factors belonging to the Trithorax group (TrxG) and insulator binding proteins, respectively.

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The genetics of egg retention and fertilization success inDrosophila: One step closer to understanding the transition from facultative to obligate viviparity

Cited by 20 publications

References 144 publications

Natural variation in theCaenorhabditis elegansegg-laying circuit modulates an intergenerational fitness trade-off

Natural variation in theCaenorhabditis elegansegg-laying circuit modulates an intergenerational fitness trade-off

Recording and reproducing the diurnal oviposition rhythms of wild populations of the soft- and stone- fruit pest Drosophila suzukii

Genome-wide temperature-sensitivity of PcG regulation and reduction thereof in temperateDrosophila melanogaster

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