Both maternal and embryonic exposure to mild hypoxia influence embryonic development of the intertidal gastropod Littorina littorea (Linnaeus, 1758)

Abstract

There is growing evidence that maternal exposure to environmental stressors can alter offspring phenotype and increase fitness. Here, we investigate the relative and combined effects of maternal and developmental exposure to mild hypoxia (65% and 74% air saturation respectively) on the growth and development of embryos of the marine gastropod Littorina littorea. Differences in embryo morphological traits were driven by the developmental environment, whereas the maternal environment and interactive effects of maternal and developmental environment were the main driver of differences in the timing of developmental events. While developmental exposure to mild hypoxia significantly increased the area of an important respiratory organ, the velum, it significantly delayed hatching of veliger larvae and reduced their size at hatching and overall survival. Maternal exposure had a significant effect on these traits, and interacted with developmental exposure to influence the time of appearance of morphological characters, suggesting that both are important in affecting developmental trajectories. A comparison between embryos that successfully hatched and those that died in mild hypoxia revealed that survivors exhibited hypertrophy in the velum and associated pre-oral cilia suggesting these traits are linked with survival in low oxygen environments. We conclude that both maternal and developmental environments shape offspring phenotype in a species with a complex, developmental life history, and that plasticity in embryo morphology arising from exposure to even small reductions in oxygen tensions impacts the hatching success of these embryos.

Insights into ontogenetic scaling and morphological variation in sharks from near-term brown smooth-hound (Mustelus henlei) embryos

“…In several shark species where multiple paternity is present, fertilisation is thought to occur over an extended period of time (Schmidt et al, 2010; Marino et al, 2015). In this scenario there may be discrepancies in the maternal provisioning that different embryos receive at a given embryogenic stage, as in matrotrophic species the nutrients provided to embryos by the mother depends to some extent on the trophic characteristics of the environmental conditions to which the mother is exposed (Olin et al, 2011; McCoy et al, 2020). The degree of body size variation in our results (Table 2) combined with the ∼10 month gestation period and seasonal migratory behaviour of M. henlei (Pérez-Jiménez and Sosa-Nishizaki, 2008) leads us to suggest that multiple paternity in this taxon likely does result in different embryos within a litter receiving different nutritional profiles from the mother at given embryogenic stages.…”

“…It is also important to consider that embryo morphology may also be influenced by prepartum environmental conditions (Kaplan and Phillips, 2006; Rodda and Seymour, 2008). Selective pressures associated with prepartum conditions could include sibling relatedness (Pfennig and Collins, 1993), constraints relating to the anatomy of the mother (Qualls et al, 1995), and even temporal variation in the environmental conditions experienced by the mother (Sale et al, 2007; McCoy et al, 2020). Each of these factors is yet to be considered from the perspective of elasmobranch taxa, representing a significant gap in our understanding of morphological evolution within this clade.…”

Effects of temperature, salinity and diet on embryonic and early larval development in Littorina littorea (Gastropoda: Littorinimorpha)

“…This value can now be used for comparisons with other L. littorea populations from different areas to investigate adaptations across the vast geographical areas this species occurs. Mccoy et al (2020) investigated L. littorea egg development under hypoxia but reported that the control group (normoxia at 14°C) reached 50% hatch after 8.8 days. Using the t 0 established it his study, this would relate to 65 DD eff , thus reasonably matching the average calculated for the current experiment (60.7 DD eff ).…”

Divergent Carry-Over Effects of Hypoxia during the Early Development of Abalone

“…Environmental hypoxia events caused by global warming and coastal eutrophication are becoming one of the most important changes in the open ocean and coastal waters worldwide. , These events can have important impacts on the abundance, survival, behavior, growth, development, and reproduction of marine organisms. − The effects of hypoxia on organisms vary by species, hypoxia severity, and duration of hypoxia as well as developmental stages of organisms. The long-term consequences of hypoxia exposure of marine organisms at their early developmental stages, including adverse physiological performance, a reduced growth rate, and changed hypoxia tolerance, have been also well demonstrated in fish, mollusk, − and other invertebrates . It is noted that the long-term effects of severe (<2 or <0.5 mg/L) and moderate (3–4 mg/L) hypoxia exposure on the hypoxia tolerance of marine organisms may be opposite and species-specific: for example, the zebrafish (Danio rerio) embryos that survive a severe hypoxia exposure (5% dissolved oxygen) or total anoxia (less than 0.5% dissolved oxygen) exhibited an increased hypoxia tolerance as larvae; however, the European sea bass (Dicentrarchus labrax) larvae that experienced a moderate hypoxia exposure (40% air saturation) exhibited lower resistance to hypoxia .…”