Biological Bulletin最新文献

AbstractA combination of receptors, co-receptors, and secreted Wnt modulators form protein complexes at the cell surface that activate one or more of the three different Wnt signaling pathways (Wnt/β-catenin, Wnt/JNK, and Wnt/Ca²⁺). Two or more of these pathways are often active in the same cellular territories, forming Wnt signaling networks; however, the molecular mechanisms necessary to integrate information from these pathways in these situations are unclear in any in vivo model system. Recent studies have implicated two Wnt binding receptor tyrosine kinases, receptor tyrosine kinase-like orphan receptor (Ror) and related-to-receptor tyrosine kinase (Ryk), in the regulation of canonical and non-canonical Wnt signaling pathways, depending on the context; however, the spatiotemporal expression of these genes in relation to Wnt signaling components has not been well characterized in most deuterostome model systems. Here we use a combination of phylogenetic and spatiotemporal gene expression analyses to characterize Ror and Ryk orthologs in sea urchin embryos. Our phylogenetic analysis indicates that both ror1/2 and ryk originated as single genes from the metazoan ancestor. Expression analyses indicate that ror1/2 and ryk are expressed in the same domains of many Wnt ligands and Frizzled receptors essential for the specification and patterning of germ layers along the early anterior-posterior axis. In addition, both genes are co-expressed with Wnt signaling components in the gut, ventral ectoderm, and anterior neuroectoderm territories later in development. Together, our results indicate that Ror and Ryk have a complex evolutionary history and that their spatiotemporal expression suggests that they could contribute to the complexity of Wnt signaling in early sea urchin embryogenesis.

AbstractThe environment experienced during embryonic development is a rich source of phenotypic variation, as environmental signals have the potential to both inform adaptive plastic responses and disrupt normal developmental programs. Environment-by-embryo interactions are particularly consequential for species with temperature-dependent sex determination, a mode of sex determination common in non-avian reptiles and fish, in which thermal cues during a discrete period of development drive the formation of either an ovary or a testis. Here we examine the impact of thermal variation during incubation in combination with developmental exposure to a common endocrine-disrupting contaminant on fitness-related hatchling traits in the American alligator (Alligator mississippiensis), a species with temperature-dependent sex determination. Using a factorial design, we exposed field-collected eggs to five thermal profiles (three constant temperatures, two fluctuating temperatures) and two environmentally relevant doses of the pesticide metabolite dichlorodiphenyldichloroethylene; and we quantified incubation duration, sex ratios, hatchling morphometric traits, and growth (9-10 days post-hatch). Whereas dichlorodiphenyldichloroethylene exposure did not generally affect hatchling traits, constant and fluctuating temperatures produced diverse phenotypic effects. Thermal fluctuations led to subtle changes in incubation duration and produced shorter hatchlings with smaller heads when compared to the constant temperature control. Warmer, male-promoting incubation temperatures resulted in larger hatchlings with more residual yolk reserves when compared to cooler, female-promoting temperatures. Together, these findings advance our understanding of how complex environmental factors interact with developing organisms to generate phenotypic variation and raise questions regarding the mechanisms connecting variable thermal conditions to responses in hatchling traits and their evolutionary implications for temperature-dependent sex determination.

AbstractAnthropogenic climate change is considered to be one of the greatest threats facing marine biodiversity. The vast majority of experimental work investigating the effects of climate change stressors on marine organisms has focused on calcifying organisms, such as corals and molluscs, where cross-generational phenotypic changes can be easily quantified. Bivalves in particular have been the subject of numerous climate change studies, in part because of their economic value in the aquaculture industry and their important roles as ecosystem engineers. However, there has been little to no work investigating the effects of these stressors on the symbionts associated with these bivalves, specifically, their shell-boring polychaete parasites. This is important to understand because climate change may shift the synergistic relationship between parasite and host based on the individual responses of each. If such a shift favors proliferation of the polychaete, it may very well facilitate extinction of host bivalve populations. In this review I will (i) provide an overview of research completed thus far on the effects of climate change stressors on shell-boring polychaetes, (ii) discuss the technical challenges of studying these parasites in the laboratory, and (iii) propose a standardized framework for carrying out future in vitro and in vivo climate change experiments on shell-boring polychaetes.

AbstractIn recent years, low-salinity events characterized by high temperatures (18-23 °C) and low-salinity waters (20‰-22‰) have increased during late spring and summer, when many marine invertebrate larvae are developing. The present study examines the effects of low-salinity events on particle ingestion for larvae of two echinoderm species, the sea star Pisaster ochraceus and the sand dollar Dendraster excentricus. Larvae were exposed to high temperatures and low salinities for 24 hours, followed by feeding on the alga Isochrysis galbana in high or low salinity for another 10 minutes. Exposing Pisaster larvae to high temperatures and low salinities, followed by feeding in low salinity, did not impair ingestion rates. In fact, these larvae ingested particles at similar and sometimes higher rates than those in the controls. In sharp contrast, a 24-hour exposure to a high temperature and low salinity, followed by continued exposure to low salinity to feed, led to a decrease in the number of particles ingested by 8-arm Dendraster larvae. Larvae of both species captured very few particles when returned to 30‰ after a low-salinity event, indicating that continuous interruption of larval feeding by low-salinity events during development could be deleterious. Sand dollar larvae may have responded negatively to low-salinity events in our experiments because they are found in protected bays, where they may seldom experience these events.

AbstractMicrobial symbionts are a common life-history character of marine invertebrates and their developmental stages. Communities of bacteria that associate with the eggs, embryos, and larvae of coastal marine invertebrates tend to be species specific and correlate with aspects of host biology and ecology. The richness of bacteria associated with the developmental stages of coastal marine invertebrates spans four orders of magnitude, from single mutualists to thousands of unique taxa. This understanding stems predominately from the developmental stages of coastal species. If they are broadly representative of marine invertebrates, then we may expect deep-sea species to associate with bacterial communities that are similar in diversity. To test this, we used amplicon sequencing to profile the bacterial communities of invertebrate larvae from multiple taxonomic groups (annelids, molluscs, crustaceans) collected from 2500 to 3670 m in depth in near-bottom waters near hydrothermal vents in 3 different regions of the Pacific Ocean (the East Pacific Rise, the Mariana Back-Arc, and the Pescadero Basin). We find that larvae of deep-sea invertebrates associate with low-diversity bacterial communities (~30 bacterial taxa) that lack specificity between taxonomic groups. The diversity of these communities is estimated to be ~7.9 times lower than that of coastal invertebrate larvae, but this result depends on the taxonomic group. Associating with a low-diversity community may imply that deep-sea invertebrate larvae do not have a strong reliance on a microbiome and that the hypothesized lack of symbiotic contributions would differ from expectations for larvae of coastal marine invertebrates.

AbstractNearshore foundation species in coastal and estuarine systems (e.g., salt marsh grasses, mangroves, seagrasses, corals) drive the ecological functions of ecosystems and entire biomes by creating physical structure that alters local abiotic conditions and influences species interactions and composition. The resilience of foundation species and the ecosystem functions they provide depends on their phenotypic and genetic responses to spatial and temporal shifts in environmental conditions. In this review, we explore what is known about the causes and consequences of adaptive genetic differentiation in marine foundation species over spatial scales shorter than dispersal capabilities (i.e., microgeographic scales). We describe the strength of coupling field and laboratory experiments with population genetic techniques to illuminate patterns of local adaptation, and we illustrate this approach by using several foundation species. Among the major themes that emerge from our review include (1) adaptive differentiation of marine foundation species repeatedly evolves along vertical (i.e., elevation or depth) gradients, and (2) mating system and phenology may facilitate this differentiation. Microgeographic adaptation is an understudied mechanism potentially underpinning the resilience of many sessile marine species, and this evolutionary mechanism likely has particularly important consequences for the ecosystem functions provided by foundation species.

AbstractInsight into how coastal organisms will respond to changing temperature and salinity regimes may be derived from studies of adaptation to fluctuating estuarine environments, especially under stressful range-edge conditions. We characterized a dynamic range boundary between two estuarine sea slugs, Alderia modesta (distributed across the North Pacific and North Atlantic) and Alderia willowi, known from southern and central California. The species overlap from Bodega Bay to San Francisco Bay, where populations are dominated by A. modesta after winter rains but by A. willowi after peak summer temperatures. Laboratory assays confirmed superior tolerance to low salinity for the northern species, A. modesta: encapsulated embryos developed at 8 ppt, larvae survived at 4-6 ppt, and adults survived repeated exposure to 2 ppt, salinities that reduced development or survival for the same stages of A. willowi. Adults did not appreciably differ in their high-temperature threshold, however. Each species showed increased tolerance to either temperature or salinity stress at its range margin, indicating plasticity or local adaptation, but at the cost of reduced tolerance to the other stressor. At its northern limit, A. willowi became more tolerant of low salinity during the winter rainy season, but also less heat tolerant. Conversely, A. modesta became more heat resistant from spring to summer at its southern limit, but less tolerant of low salinity. Trade-offs in stress tolerance may generally constrain adaptation and limit biotic response to a rapidly changing environment, as well as differentiating species niches.

AbstractThe diversity and consequences of development in marine invertebrates have, for a long time, provided the opportunity to understand different evolutionary solutions to living in variable environments. However, discrete classifications of development can impede a full understanding of adaptation to variable environments when behavioral, morphological, or physiological flexibility and variation exist within traditionally defined modes of development. We report here novel behavioral variability in hatchlings of a marine gastropod, the Florida crown conch (Melongena corona), that has broad significance for understanding the correlated evolution of development, dispersal, and reproductive strategies in variable environments. All hatchlings crawl away from egg capsules after emergence as larval pediveligers. Some subsequently swim for a brief period (seconds to minutes) before crawling again. From detailed observations of 120 individuals over 30 days, we observed 28 (23.3%) hatchlings swimming at least once (8%-50% per maternal brood). The propensity to swim was unrelated to time spent encapsulated or size at hatching and lasted for 22 days. We manipulated hypothesized environmental cues and found that the proportion of hatchlings that swam was highest in the absence of cues related to habitat or juvenile food and lowest when only habitat cues were present. The relative growth rate of hatchlings was highest when habitats contained a putative juvenile food source. About 44% of hatchlings were competent to metamorphose at emergence but did not metamorphose at this time in the lab or the field. The rate of metamorphosis increased with age and depended on the presence of unknown cues in the field. Crawl-away larvae with prolonged swimming ability may be an adaptation to balance the unpredictable risks of exclusively benthic or pelagic development and to allow the option to disperse to higher-quality habitat.

AbstractUnderstanding how species may respond to climate change is of paramount importance. Species that occupy highly heterogenous environments, such as intertidal zone estuarine habitats, provide an ideal test case for examining phenotypic and genomic adaptations to different environmental conditions, which may influence their response to rapidly shifting climatic conditions. The California coast is projected to experience changes in both temperature and salinity, which currently vary seasonally and latitudinally. Using comparative transcriptomics, I documented patterns of positive selection between the northern-dwelling planktotrophic sacoglossan sea slug Alderia modesta, which is remarkably tolerant of low temperatures and low salinities, and its southern congener Alderia willowi, which exhibits a striking flexibility for larval type in response to seasonally shifting changes in temperature and salinity. Out of over 4000 1-to-1 orthologous genes, I found a signal of positive selection between A. willowi and A. modesta for genes involved in cell membrane and cell transport, particularly ion homeostasis (aquaporin), cell-cell signal transduction, and phosphorylation (reduced nicotinamide adenine dinucleotide [NADH] dehydrogenase). Positive selection for ion homeostasis in A. modesta has implications for its ability to tolerate the lower salinity of its northern range, and in A. willowi substitutions in NADH may assist in the high temperature tolerance of its southern California habitats. Identifying these candidate genes enables future studies of their functionalization as we seek to understand the relationship between phenotype and genotype in species whose phenotypes are influenced by environmental conditions.