The transcriptomic signature of cyclical parthenogenesis

Abstract

Cyclical parthenogenesis, where females can engage in sexual or asexual reproduction depending on environmental conditions, represents a novel reproductive phenotype that emerged during eukaryotic evolution. The fact that environmental conditions can trigger cyclically parthenogens to engage in distinct reproductive modes strongly suggests that gene expression plays a key role in the origin of cyclical parthenogenesis. However, the genetic basis underlying cyclical parthenogenesis remains understudied. In this study we characterize the female transcriptomic signature of sexual vs. asexual reproduction in the cyclically parthenogenetic microcrustacean Daphnia pulex and D. pulicaria. Our analyses of differentially expressed genes, pathway enrichment, and GO term enrichment clearly show that compared to sexual reproduction the asexual reproductive stage is characterized by both the under-regulation of meiosis and cell-cycle genes and the up-regulation of metabolic genes. We suggest that the under-regulation of meiosis and cell-cycle genes is responsible for the origin of parthenogenesis from meiosis, whereas differentially expressed metabolic genes may mediate choice of asexual vs. sexual reproductive pathway. Furthermore, our analyses identify some cases of divergent expression among gene family members (e.g., doublesex, NOTCH2) associated with asexual or sexual reproductive stage, suggesting potential functional divergence among gene family members.

Reproduction-associated pathways in females of gibel carp (Carassius gibelio) shed light on the molecular mechanisms of the coexistence of asexual and sexual reproduction

“…In accordance with our results, gynogenetic P. formosa was shown to underexpress meiosis-related genes, including sbk3, setd7 and stk32c, compared to its supposed sexual ancestors (19). Similarly, in cyclically parthenogenetic Daphnia, meiosis-related genes, including genes related to the spindle assembly checkpoint, the APC, and meiosis chromosome segregation, were upregulated during sexual reproduction (71). In particular, spo11, which encodes a topoisomerase involved in chromosomal recombination during the meiotic prophase, was also described as an important player in the meiosis-to-parthenogenesis transition in pea aphid (87), although it was not reported in asexual P. formosa (19).…”

“…It is noteworthy that members of the same gene family can be up-or downregulated, such as members of the zona pellucida and F-box families. Such divergent expression, also reported in Daphnia (71), may suggest functional divergence among members of the same multigenic families.…”

Efficient CRISPR genome editing and integrative genomic analyses reveal the mosaicism of Cas-induced mutations and pleiotropic effects ofscarletgene in an emerging model system

“…Among these emerging systems, Daphnia has excellent potential for genomic functional studies, largely thanks to the wealth of knowledge accumulated from decades of research on their evolution/adaptation, ecology, toxicology, phenotypic plasticity, and response to environmental factors (Altshuler et al 2011). Since the development of first-generation Daphnia genomic tools (Colbourne et al 2011), researchers have identified a large number of candidate genes responsible for various biological processes, such as adaptation to freshwater salinization (Wersebe and Weider 2023), heavy metal contamination (Shaw et al 2007), the origin of obligate parthenogenesis and cyclical parthenogenesis (Xu et al 2015; Xu et al 2022; Huynh et al 2023; Snyman and Xu 2023), and adaptation to ecologically distinct habitats (Ye et al 2023), which are ready to be further interrogated for functional insights.…”

On the Origin of Obligate Parthenogenesis inDaphnia pulex

“…These results suggests that the origin of obligate parthenogenesis from meiosis is likely caused by the downregulation of key meiosis and cell cycle genes, and an upregulation of metabolism. Interestingly, when comparing the gene expression patterns between early subitaneous egg and early resting egg production within individual CP D. pulex and D. pulicaria isolates (Figure 2B) , meiosis and cell cycle genes were also found to be downregulated while metabolic, and biosynthesis genes were upregulated in early subitaneous egg development (i.e., parthenogenesis) compared to resting egg production (i.e., meiosis) in both species (Huynh et al . 2021).…”

“…These results suggests that the origin of obligate parthenogenesis from meiosis is likely caused by the downregulation of key meiosis and cell cycle genes, and an upregulation of metabolism. Interestingly, when comparing the gene expression patterns between early subitaneous egg and early resting egg production within individual CP D. pulex and D. pulicaria isolates (Figure 2B), meiosis and cell cycle genes were also found to be downregulated while metabolic, and biosynthesis genes were upregulated in early subitaneous egg development (i.e., parthenogenesis) compared to resting egg production (i.e., meiosis) in both species (Huynh et al 2021). Together, the results from these two transcriptomic studies strongly suggest that parthenogenesis in both OP (resting egg production) and CP (subitaneous egg production) isolates are associated with a downregulation of meiosis and cell cycle genes and an upregulation of metabolic and biosynthesis genes, which may play essential roles in triggering parthenogenesis.…”