Capital Breeding in a Diapausing Copepod: A Transcriptomics Analysis

Abstract

Capital breeders must balance the energetic requirements of cellular function and the cost of reproduction. The subarctic copepod Neocalanus flemingeri, a small planktonic crustacean, depends on a short annual phytoplankton bloom to acquire the energy needed to support a non-feeding adult female that enters a period of diapause prior to spawning 5 to 7 months later. After emergence from diapause, the reproductive program takes 2 months starting with germline development. In this study, the regulation of genes involved in energy utilization and cellular maintenance were investigated using RNA-Seq as females progressed from diapause to end-of-life. Hierarchical clustering of expression profiles from 61 individual females identified four major transitions in transcriptional profiles along a timeline spanning from diapause to spawning and postreproduction. The clusters were analyzed statistically for differential gene expression followed by functional analyses. The transition from diapause to post-diapause (early to mid-oogenesis) was characterized by the up-regulation of genes involved in cellular homeostasis, glycolysis and lipid catabolism. As females approached spawning genes involved in cellular homeostasis, like innate immunity became down-regulated. Genes involved in protein ubiquitination and programmed cell death became up-regulated as females started to spawn. Gene expression patterns suggest that energy allocation and utilization is highly dynamic in N. flemingeri during the progression of the reproductive period. Major changes in the expression of genes involved in cellular homeostasis, metabolic processes and autophagy were linked to stages of egg maturation. Changes in gene expression that marked the transition from diapause to post-diapause were similar to those reported in other arthropods that resume feeding after emergence from diapause. As egg maturation progressed, gene expression patterns indicate that resources became concentrated on provisioning eggs, while being diverted away from cellular homeostasis. The data suggest that in N. flemingeri genes are regulated such that organismal function and sources of energy are synchronized with stages of egg maturation to optimize the exploitation of finite resources. The existence of mechanisms that regulate fecundity to match the availability of stored resources could reduce reproductive failure in this species.

Physiological acclimatization in high‐latitude zooplankton

“…Neocalanus flemingeri , the focus of this study, is a filter feeder that consumes a wide range of single‐celled autotrophs and heterotrophs with a preferred food size >20 µm (Dagg et al, 2009; Liu et al, 2008). This species has nonfeeding adults and depends on the spring phytoplankton bloom to store enough resources (“capital”) to fuel both diapause and reproduction (Lenz & Roncalli, 2019; Roncalli et al, 2020).…”

Lipid metabolism in Calanus finmarchicus is sensitive to variations in predation risk and food availability

“…Exposure to oil pollution has been observed to disrupt lipid catabolism 32 , indicating additional sensitivity to anthropogenic disturbances. In Neocalanus flemingeri lipid catabolism genes were in contrast upregulated towards the end of diapause (which occurs in adults), and did not become reduced 41 . This underlines species differences and the complexity of energetic metabolism in diapausing zooplankton species.…”

Annual transcriptome of a key zooplankton species, the copepod Calanus finmarchicus

“…Our study presents a significant contribution in providing the first in situ annual transcriptomic resource of a key zooplanktonic species, the copepod C. finmarchicus. This is significant since seasonal transcriptomic investigations in wild marine organisms are rare (Clark et al, 2013;Häfker et al, 2018;Lenz, Lieberman, et al, 2021;Roncalli et al, 2018Roncalli et al, , 2020Roncalli et al, , 2021Semmouri et al, 2020;Tarrant et al, 2014). The proposed dataset is of interest and of high quality due to the unique and rigorous temporal resolution of sampling spanning the entire year and thereby facilitating rhythmic analysis (Thaben & Westermark, 2014).…”

“…Considering the key position of lipid‐rich copepods in the food web (Archibald et al, 2019 ; Beaugrand et al, 2003 ; Berge et al, 2012 ; Prokopchuk & Sentyabov, 2006 ), such mismatches may ultimately have consequences on energy flow pathways in ecosystems and carbon sequestration (Friedland et al, 2018 ). While our current understanding of the life cycle and ecology of copepods has emerged mostly from population dynamics and physiological studies (Baumgartner & Tarrant, 2017 ; Lenz & Roncalli, 2019 ), seasonal investigations on the transcriptional level are still rare and fragmentary (Clark et al, 2013 ; Häfker et al, 2018 ; Lenz, Lieberman, et al, 2021 ; Lenz, Roncalli, et al, 2021 ; Roncalli et al, 2018 , 2020 , 2021 ; Semmouri et al, 2020 ; Tarrant et al, 2014 ), as too are the processes controlling the timing of the annual life cycle (Baumgartner & Tarrant, 2017 ; Lenz & Roncalli, 2019 ).…”