Offspring size and maternal environments mediate the early juvenile performance of two congeneric whelks

Abstract

Offspring size variation can have pervasive ecological and evolutionary implications for both offspring and mother, affecting an organism's performance throughout its life. Using 2 marine intertidal whelk species Cominella virgata and C. maculosa as model organisms, we examined how different maternal environments and contrasting hatchling size influence juvenile performance. The average size of field-collected hatchlings greatly differed between the species and at different scales of variation (i.e. among sites). Species-specific differences in hatching size were reflected in juvenile performance. Overall, C. virgata with larger hatchlings (~3 mm), exhibited faster growth rates and higher survival than the smaller C. maculosa (~1.5 mm). Desiccation treatment did not affect the performance of fed juveniles; however, large hatchlings had higher growth rates than small conspecifics for both species. Starved hatchlings of both species performed more poorly than fed ones; however, species-specific and size differences were less significant for the evaluated traits, suggesting a non-size-related allocation of resources and similar resource utilization during starvation conditions (i.e. within species). As has been described for many taxa, large offspring often perform better than small conspecifics; however, because this performance is likely context-dependent, understanding the importance of different scales of variation is crucial for determining when variation in size is an advantage or a disadvantage in terms of an organism's performance. KEY WORDS: Progeny size · Reproductive strategies · Environmental variation · Phenotypic plasticity · Offspring size-fitness · Cominella Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 459: [73][74][75][76][77][78][79][80][81][82][83] 2012 to either non-adaptive stochastic variation in provisioning or to a maternal bet-hedging strategy in unpredictable environments (see Kamel et al. 2010).The ability of mothers to anticipate the environment that their offspring will experience may therefore mediate variation in offspring size. When mothers are able to predict their offspring's environment, the expectation is that plasticity in mean offspring size will be favored ('anticipatory' maternal effects;Marshall & Uller 2007). Conversely, when mothers are unable to predict the environment, the expected outcome is that increases in the variation of offspring size will ensure that some offspring will be optimal for the environment (Crean & Marshall 2009). Regardless of the strategy, the division of finite reproductive resources should ultimately result in an optimal equilibrium between the offspring fitness and the maximization of the parental fitness, and therefore, simple models have typically suggested that as the relationship between progeny size and progeny fitness changes, the optimal size of progeny is also expected to change as environmental conditions vary (Fox 2000, Walker et al. 2003. Examples provided by Allen et al. (...

Differential vulnerability to predation in two sympatric whelks is mediated by juvenile traits

“…A recent study of differently sized juveniles of C. virgata and C. maculosa kept in laboratory conditions also showed similar within‐ and between‐species differences in performance, with larger hatchlings of both species being, in most cases, less vulnerable to the stressors evaluated (desiccation and starvation) compared with smaller hatchlings (Carrasco et al. ). Together, these findings suggest that inter‐ and intraspecific differences in per‐offspring investment will not only mediate the performance of these juvenile whelks when faced with predators (as shown here), but will also affect growth rates and survival under different physical stressors.…”

“…Recent studies on juvenile performance for both species showed that growth rates of C. maculosa (~0.02 mm d −1 ) were nearly half those of C. virgata (~0.04 mm d −1 ) during the first month after hatching in laboratory conditions (Carrasco et al. ), and therefore, it is not surprising that juveniles of C. maculosa might require at least two more months to eventually reach the size refuge of ~4.8 mm SL and ~0.11 mm shell thickness observed in the less vulnerable 2‐month‐old juveniles of C. virgata .…”

“…Several studies across a variety of taxa and habitats have shown that larger offspring often perform better than smaller conspecifics in terms of growth rate, probability of survival, reproductive success, outcome of competition, and vulnerability to predation [e.g., gastropods (Spight ; Gosselin ; Moran & Emlet ; Carrasco et al. ), mussels (Phillips ), barnacles (Thiyagarajan et al. ), ascidians (Marshall et al.…”

Phylogeography of the whelk genusCominella(Gastropoda: Buccinidae) suggests long-distance counter-current dispersal of a direct developer

“…Successful long‐distance dispersal might appear unlikely in Cominella because, similar to most buccinid whelks, all Cominella species whose development has been studied have been shown to undergo direct development (Anderson, ; Pilkington, ; van der Sman, Phillips & Pfister, ; Carrasco et al ., ) and their natural habitats do not usually include rafting materials. We note, however, that Bouchet & Warén () recorded buccinid egg capsules on pumice and Morley () has observed C. glandiformis egg capsules on both driftwood and oyster ( Saccostrea cucullata ) clumps.…”

“…Currently, 20 Cominella species are recognized, all of which are endemic to one of New Zealand (13 species), Norfolk Island (one species) or mainland Australia and Tasmania (six species) (Wilson ; Spencer et al ., ). This reciprocal species‐level endemism is in keeping with the high level of endemism (85%) typically observed among New Zealand molluscs (Spencer et al ., ) and reflects both the long period that New Zealand has been isolated from other land masses and the whelks' limited dispersal ability, a result of direct development (Anderson, ; Carrasco, Phillips & Perez‐Matus, ), as well as a low potential for rafting (see below).…”