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Decapod crustacean larval developmental plasticity and the evolution of lecithotrophy and abbreviated development
No full textWithin the marine environment, the diverse development modes among marine invertebrate taxa follow a macro-ecological pattern across latitude. Generally, across the latitudinal gradient from the tropics to the poles, larval development becomes increasingly independent of external food resources. Low latitude species are fecund and produce relatively poorly provisioned eggs, which develop into swimming and feeding larvae. This mode of development becomes increasingly scarce with increasing latitude, whilst development from large eggs (produced in low numbers) into larvae, which are non-feeding, becomes increasingly prevalent. From the tropics to the poles, there is an increasing mismatch between the longer periods required for larval development (resulting from increasing cold) and the shorter periods of food availability (resulting from increasing seasonality). This macro-ecological trend in development modes results from the convergent evolution of diverse taxa, which have adapted to high latitude environments in much the same way: through producing larvae which develop independently of external food resources. Developmental plasticity during the larval phase is a mechanism by which larvae are able to cope better with unfavourable conditions or variations in their environment. Critically, the interaction between per offspring investment (POI; the quantity and quality of resources allocated to offspring) and developmental plasticity, and the role of this interaction in the evolution of larval development modes, is little considered or studied. Experiments comprising this thesis assess the potential role of this interaction in the evolution of abbreviated and lecithotrophic development within decapod crustaceans, and the establishing of the macro-ecological trend in development outlined above. Experiments used the palaemonine shrimp, Palaemonetes varians, which inhabits temperate, salt marsh, and peripheral brackish water, as a study species. Palaemonine Abstract ii shrimp originated from a tropical marine clade and extant species are found in marine, brackish, and fresh water environments. The evolutionary transition from marine to fresh water has involved life history adaptations in development mode within this group. As species occupy differing habitats along this environmental gradient, this group has been used to study evolutionary adaptations along the environmental gradient from marine to fresh water.Sampling of a wild population of P. varians from Lymington salt marsh (Hampshire, UK) revealed the highly variable environment that this species inhabits. POI within this population varied inter- and intra-annually, though these variations could not be correlated with variations in environmental temperatures. Larvae hatch with significant yolk reserves and can be considered facultative lecithotrophic in the first and second larval instar, and planktotrophic from the third larval instar. Larval development was successful at temperatures between 15 and 30 °C and temperature-mediated developmental plasticity was observed; at higher temperatures, larvae increasingly developed through fewer larval instars. Development through fewer larval instars resulted in more rapid development, but development to a lesser juvenile dry weight at settlement. Consequently, this developmental plasticity may have ecological implications. Developmental plasticity was also influenced by the energy content of larvae at hatching (as proxy for POI). Larvae with greater energy content developed through fewer larval instars at all temperatures, indicating that higher POI buffers larvae against poor conditions during development. Greater energy content also enabled larvae to tolerate starvation for longer and to develop to more advanced larval stages in the absence of food.Developmental plasticity within decapod crustaceans enables larvae to tolerate unfavourable conditions during development. Interestingly, it maximises the potential fitness benefits provided by POI by enabling larvae to settle as juveniles earlier, though at a smaller size. The interaction between POI and developmental plasticity forms a ‘pre-adaptation’ for the evolution of abbreviated development. The results presented in this thesis indicate that, indeed, the evolutionary transition to abbreviated development and lecithotrophy is based on selection for increasing POI. The abbreviation of development associated with increasing POI arises through developmental plasticity in larval instar number
Energetic adaptations to larval export within the brackish living palaemonine shrimp, Palaemonetes varians
No full textDecapod crustaceans have repeatedly colonised brackish, freshwater, and terrestrial environments. Many decapods, which inhabit brackish and freshwater habitats, export larvae into estuarine and coastal areas where conditions for larval development may be better. In this study, we assess the starvation resistance, biochemical composition and respiration rate during larval development, and the effects of temperature on these factors within the brackish living palaemonine shrimp, Palaemonetes varians. Our results demonstrate that P. varians is highly resistant to starvation and may be considered facultative lecithotrophic in its first and second larval instars and planktotrophic from its third instar. This high starvation resistance is associated with a relatively large size, high carbon content (~45%) and C:N ratio (~4.2), and visible yolk reserves at hatching. These energy reserves are interpreted as an adaptation to the exportation of larvae from peripheral adult environments into mid and lower estuarine waters. Respiration rates varied with the moult cycle and were similar between fed and unfed larvae, suggesting that starved larvae do not suppress their metabolism as an energy saving strategy. Despite higher respiration rates at higher temperatures, energy loss throughout development (estimated from respiration rates) increased with decreasing temperature, whilst larval growth and development rates decreased with increasing temperature. High energy reserves at hatching, as within Palaemonetes varians, is an important life history adaptation in the colonisation of brackish and freshwaters, initially enabling the exportation of larvae from adult environments and eventually enabling lecithotrophy and direct development
Per offspring investment implications for crustacean larval development: evolutionary insights into endotrophy and abbreviated development
No full textAt the inter-specific level, Per Offspring Investment (POI) is associated with larval development mode and follows a macro-ecological trend within the marine environment; higher POI and its associated greater degree of endotrophy and abbreviated development is found in cooler, high latitude regions. Here, the implications of between-brood-variation in hatchling energy content (measured as carbon mass) on larval starvation resistance and developmental plasticity within the caridean shrimp, Palaemonetes varians, were assessed. Results demonstrate that greater POI provides increased endotrophy and the potential for abbreviated development. In the absence of food, P. varians larvae from broods of higher hatchling energy content developed to more advanced larval stages and survived for longer before succumbing to starvation. In the presence of food, P. varians larvae from broods of higher hatchling energy content developed through fewer larval instars, showed higher growth rates, and had shorter development times. Also, for larvae developing through the same number of larval instars, larvae from broods of higher hatchling energy content developed to greater juvenile dry weight. These data support the hypothesis that macro-ecological trends in development mode are driven by POI; environmentally mediated phenotypic plasticity in POI may therefore permit the evolution of the diverse and complex life cycles observed in the marine environment
Variable shrimp in variable environments: Reproductive investment within Palaemon varians
No full textThe maternal environment may influence the quantity and quality of resources invested in offspring (per-offspring provisioning) and this trait, in turn, affects larval fitness and may carry-over into early juvenile life. Here, per-offspring investment was measured across three consecutive breeding seasons for the caridean shrimp, Palaemon varians. Egg and hatchling larval dry weight as well as hatchling larval biochemical composition were measured. Results indicate that egg volume is positively correlated with dry weight, but egg volume as a proxy for dry weight should be used with caution. Correlations were identified between per-offspring investment and average breeding season temperature, but the period over which temperature was averaged was important to whether these correlations were positive or negative, highlighting the complexity of identifying environmental influence on phenotypic traits. The most important factor determining offspring size and per-offspring investment was maternal size, which may be influenced by the environment as carapace length varied significantly between breeding seasons. These data demonstrate variation in egg and larval composition, related to maternal size, which will affect early life traits and survivorship for P. varians
The influence of Per Offspring Investment (POI) and starvation on larval developmental plasticity within the palaemonid shrimp, Palaemonetes varians
No full textAt the inter-specific level, per offspring investment (POI), degree of abbreviated development, and lecithotrophic potential all increase with increasing latitude and freshwater penetration among crustaceans. These traits are considered adaptations to conditions of decreasing growth potential. We hypothesis that the relationship between POI and abbreviated development also occurs at the intra-specific level. We studied the caridean shrimp, Palaemonetes varians, to investigate the hypothesis that under food-limited conditions, higher POI enables development through fewer larval instars. Larvae from broods of greater POI (measured as hatchling dry weight, W, and categorised as ‘small’, ‘medium’, or ‘large’) generally developed through fewer larval instars. With increasing starvation period, larval development time increased and larval growth rate, juvenile W, juvenile carbon mass, and juvenile C:N ratio all decreased. Larval development time decreased with increasing larval W category. In contrast larval growth rate, juvenile W, juvenile carbon mass, and juvenile C:N ratio all increased with increasing larval W categorys. There were no interactions between starvation treatment and larval W category for any larval or juvenile trait, except larval development time. These results are consistent with the relationship between POI and larval instar number (abbreviation of development) at the inter-specific level and support the concept that macro-ecological trends in development modes at the inter-specific level may be driven by selection occurring on POI at the intra-specific level
The implications of temperature-mediated plasticity in larval instar number for development within a marine invertebrate, the shrimp Palaemonetes varians
No full textVariations in larval instar number are common among arthropods. Here, we assess the implications of temperature-mediated variations in larval instar number for larval development time, larval growth rates, and juvenile dry weight within the palaemonid shrimp, Palaemonetes varians. In contrast with previous literature, which focuses on terrestrial arthropods, particularly model and pest species often of laboratory lines, we use wild shrimp, which differ in their life history from previous models. Newly-hatched P. varians larvae were first reared at 5, 10, 17, 25, and 30°C to assess their thermal scope for development. Larvae developed at 17, 25, and 30°C. At higher temperatures, larvae developed through fewer larval instars. Two dominant developmental pathways were observed; a short pathway of four instars and a long pathway of five instars. Longer developmental pathways of six to seven instars were rarely observed (mostly at lower temperatures) and consisted of additional instars as ‘repeat’ instars; i.e. little developmental advance over the preceding instar. To assess the implications of temperature-mediated variation in larval instar number, newly-hatched larvae were then reared at 15, 20, and 25°C. Again, the proportion of larvae developing through four instars increased with temperature. At all temperatures, larval development time and juvenile dry weight were greater for larvae developing through five instars. Importantly, because of the increasing proportion of larvae developing through four instars with increasing temperature, larval traits associated with this pathway (reduced development time and juvenile dry weight) became more dominant. As a consequence of increasing growth rate with temperature, and the shift in the proportion of larvae developing through four instars, juvenile dry weight was greatest at intermediate temperatures (20°C). We conclude that at settlement P. varians juveniles do not follow the temperature-size rule; this is of importance for life-history ecology in response to environmental change, as well as for aquaculture applications
Phospholipid fatty acids are correlated with critical thermal tolerance but not with critical pressure tolerance in the shallow-water shrimp Palaemon varians during sustained exposure to low temperature
No full textSome extant deep-sea shrimp are known to be descended from shallow-water ancestors that adapted to environmental conditions (constant low temperature and high hydrostatic pressure) in the deep sea. During acclimation to low temperature and high hydrostatic pressure representative of the deep-sea, critical thermal tolerance decreases and critical pressure tolerance increases in the shallow-water shrimp Palaemon varians. It has been suggested that these shifts may depend in part on adjustments to phospholipid fatty acid composition and/or metabolic adjustments. Here, we present evidence that metabolic rate does not change during sustained exposure to low temperature (5°C) in the shallow-water shrimp Palaemon varians, and that metabolic rate and acute environmental tolerances are not correlated during sustained exposure to low temperature, suggesting that standard metabolic rate does not affect acute environmental tolerances. In contrast, we present evidence that phospholipid fatty acid composition does shift during sustained exposure to low temperature. Desaturation of fatty acids during sustained exposure to low temperature supports the suggestion that cell lipid bilayer homeoviscous modifications are important in low temperature acclimation. Shifts in several individual phospholipid fatty acids during sustained low temperature exposure are correlated with critical thermal tolerance. Exploring the greater complexity apparent in the responses of these phospholipid fatty acids to sustained low temperature exposures suggests a potential homeostatic impact moderating adverse impacts on nervous system function. However, shifts in phospholipid fatty acids are not correlated with critical pressure tolerance during exposure to low temperature, suggesting that shifts in critical pressure tolerance are related to modifications other than cell lipid bilayer composition.<br/
Intraspecific variability in larval development in the lithodine crab Lithodes maja
No full textInterspecific comparison of larval duration in lecithotrophic deep-water lineage lithodine king crabs suggests that faster development at a given temperature is associated with greater energetic reserve utilisation. Similarly, intraspecific comparison using data from two different studies has suggested that faster development at a given temperature is associated with greater energetic reserve utilisation in the deep-water-lineage lithodine Lithodes maja. To assess intraspecific covariation in duration of larval development and energetic resource utilisation more robustly, we examined larval development parameters (survival, duration of development, and energetic reserve utilisation) in broods from three different captive-mated females of the northern stone crab L. maja incubated and maintained under identical conditions at 6 °C. Larval survival was similar among broods but duration of development differed. Energetic reserve utilisation also differed among broods with the depletion of C mass and N mass appearing greater in faster developing larvae. The greater energetic cost of more rapid development may contribute to selection pressure for increased per-offspring investment during adaptation to low temperature and high hydrostatic pressure in lithodid species. Although the limited number of broods examined prevents definitive conclusions, results presented here suggest potential links between duration of development and energetic reserve utilisation, warranting further exploration of this relationship
The consequences of daily cyclic hypoxia on a European grass shrimp: from short-term responses to long-term effects
No full text1.Salt marshes are a key coastal environment for their important role as nursery habitats for marine and estuarine fish and crustaceans. Salt marshes are variable environments where species can experience daily cyclic hypoxic stress, characterized by profound variations in oxygen partial pressure (pO2) from supersaturated conditions (~42kPa) to extremely hypoxic conditions (~3kPa) in ~12‐hours.
2.Here, under laboratory conditions, we assessed the physiological consequences of exposing the shrimp Palaemon varians, a species commonly found in the salt marshes of northern Europe, to the daily cyclic hypoxic regime currently experienced in its habitat in August (7.1±1.8 hours day−1 below 4.0kPa). In the laboratory adults were kept at water pO2 <4.5kPa for 7‐hours each night and in normoxic conditions for the rest of the time.
3.We recorded an acceleration of P. varians’ moult cycle, which was 15% shorter in animals kept in cyclic hypoxia compared to animals in normoxia. Similarly, the pattern of expression of two cuticular proteins over an entire moult cycle indicated an effect of cyclic hypoxia on moult stage‐related genes. After 16 days, morphological changes to the gills were detected, with shrimps in cyclic hypoxia having a 13.6% larger lamellar surface area (measured in μm2/mg animal) than normoxic animals, which could improve gas exchange capacity. Overall, phenotypic and morphological data indicate that faster moulting is triggered in response to cyclic hypoxia, with the benefit that gill modifications can be prompted more rapidly in order to meet oxygen requirements of the body.
4.On the first experimental day, in cyclic hypoxic exposed animals, we recorded a 50% decrease in feeding rates (during hypoxic conditions) in comparison to normoxic animals. Similarly, ammonium excretion was reduced by 66‐75% during the 1st and 21st experimental day. Body size was reduced by ~4% after 28 days. Females that reproduced in cyclic hypoxic conditions reduced the amount of yolk in each egg by ~24%. Overall, results underline how, in a decapod shrimp living in a key coastal environment, many physiological parameters are impaired by a cyclic hypoxic regime that is currently found in its natural habitat
Temperature adaptation in larval development of lithodine crabs from deep-water lineages
No full textAdaptations in per-offspring investment and larval development are considered to have been crucial to the global radiation of deep-water lineages of lithodine crabs (Lithodinae). Temperature is proposed to drive latitudinal trends in energy provisioning of eggs in marine invertebrates, mediated by thermally dependent intraspecific plasticity in per-offspring investment. Consequently, a changing climate may be expected to directly affect larval provisioning. We analysed available data to examine any differences in per-offspring investment and larval development among deep-water lineage lithodines. Although data are few, interspecific differences in the thermal scope of deep-water-lineage lithodine larvae appear coupled with differences in biogeography. This coupling suggests environmental temperature influences larval thermal scope. Lithodine phylogeography suggests that larval cold-eurythermy in deep-water-lineage lithodines is a derived trait that has evolved in relatively warm and variable subantarctic shallow water. Therefore, we hypothesise that capacity to adapt to warmer and more variable environmental conditions may afford deep-water-lineage lithodines some resilience to ocean warming, depending on the rates of environmental and adaptive change. Interspecific comparisons also suggest that larval duration and per-offspring investment are positively correlated. Faster development at a given temperature is associated with higher respiration rates and greater energetic reserve utilisation. Therefore, we hypothesise that selection pressure for contrasting metabolic adaptations in different thermal environments contributes to shifts in larval duration and per-offspring investment
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