Climate change threatens symbiotic cnidarians’ survival by causing photosymbiosis breakdown in a process known as bleaching. Direct effects of temperature on cnidarian host physiology remain difficult to describe because heatwaves depress symbiont performance, leading to host stress and starvation. The symbiotic sea anemone Exaiptasia diaphana provides an opportune system to disentangle direct vs. indirect heat effects on the host, since it can survive indefinitely without symbionts. We tested the hypothesis that heat directly impairs cnidarian physiology by comparing symbiotic and aposymbiotic individuals of two laboratory subpopulations of a commonly used clonal strain of E. diaphana, CC7. We exposed anemones to a range of temperatures (ambient, +2°C, +4°C, +6°C) for 15–18 days, then measured their symbiont population densities, autotrophic carbon assimilation and translocation, photosynthesis, respiration, and host intracellular pH (pHi). Symbiotic anemones from the two subpopulations differed in size and symbiont density and exhibited distinct heat stress responses, highlighting the importance of acclimation to different laboratory conditions. Specifically, the cohort with higher initial symbiont densities experienced dose-dependent symbiont loss with increasing temperature and a corresponding decline in host photosynthate accumulation. In contrast, the cohort with lower initial symbiont densities did not lose symbionts or assimilate less photosynthate when heated, similar to the response of aposymbiotic anemones. However, anemone pHi decreased at higher temperatures regardless of cohort, symbiont presence, or photosynthate translocation, indicating that heat consistently disrupts cnidarian acid-base homeostasis independent of symbiotic status or mutualism breakdown. Thus, pH regulation may be a critical vulnerability for cnidarians in a changing climate.
more »
« less
A symbiotic oyster in a shrimp burrow: phylogenetic position of Anomiostrea within the Ostreidae (Bivalvia)
ABSTRACT The ostreid genus Anomiostrea Habe & Kosuge, 1966, is monotypic for A. coralliophila Habe, 1975, which is known as a symbiont inhabiting the burrow of the ghost shrimp Neocallichirus jousseaumei (Nobili, 1904), but despite this unusual habit among oysters its phylogenetic position within the Ostreidae remained unknown. Using specimens collected from two distant localities of the Indo-Pacific, Oman and Japan, we compared shell morphology of these specimens with the holotype and assessed their phylogenetic relationships based on DNA sequence data from two mitochondrial and two nuclear genes. The genetic distance in cytochrome c oxidase subunit I between the specimens from Japan and Oman was 5.5%, indicating substantial geographic differentiation. Our molecular phylogenetic results suggest that A. coralliophila is sister to Ostrea algoensis G. B. Sowerby II, 1871, an oyster from rocky shores in South Africa, and both are closely related to other Ostrea species. This confirms assignment of Anomiostrea to Ostreinae and suggests that this burrow-wall symbiont evolved from typical rocky-shore oysters. Moreover, A. coralliophila was not monophyletic with another symbiotic ostreid Ostrea permollis G. B. Sowerby II, 1871, nor with other symbiotic oysters, indicating that the symbiotic habit evolved multiple times in the Ostreinae.
more »
« less
- Award ID(s):
- 1856245
- PAR ID:
- 10548716
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Molluscan Studies
- Volume:
- 90
- Issue:
- 4
- ISSN:
- 0260-1230
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Inducible prey defences occur when organisms undergo plastic changes in phenotype to reduce predation risk. When predation pressure varies persistently over space or time, such as when predator and prey co‐occur over only part of their biogeographic ranges, prey populations can become locally adapted in their inducible defences. In California estuaries, native Olympia oyster (Ostrea lurida) populations have evolved disparate phenotypic responses to an invasive predator, the Atlantic oyster drill (Urosalpinx cinerea). In this study, oysters from an estuary with drills, and oysters from an estuary without drills, were reared for two generations in a laboratory common garden, and subsequently exposed to cues from Atlantic drills. Comparative proteomics was then used to investigate molecular mechanisms underlying conserved and divergent aspects of their inducible defences. Both populations developed smaller, thicker, and harder shells after drill exposure, and these changes in shell phenotype were associated with upregulation of calcium transport proteins that could influence biomineralization. Inducible defences evolve in part because defended phenotypes incur fitness costs when predation risk is low. Immune proteins were downregulated by both oyster populations after exposure to drills, implying a trade‐off between biomineralization and immune function. Following drill exposure, oysters from the population that co‐occurs with drills grew smaller shells than oysters inhabiting the estuary not yet invaded by the predator. Variation in the response to drills between populations was associated with isoform‐specific protein expression. This trend suggests that a stronger inducible defence response evolved in oysters that co‐occur with drills through modification of an existing mechanism.more » « less
-
Summary Holobiont phenotype results from a combination of host and symbiont genotypes as well as from prevailing environmental conditions that alter the relationships among symbiotic members. Corals exemplify this concept, where shifts in the algal symbiont community can lead to some corals becoming more or less thermally tolerant. Despite linkage between coral bleaching and disease, the roles of symbiotic bacteria in holobiont resistance and susceptibility to disease remains less well understood. This study thus characterizes the microbiome of disease‐resistant and ‐susceptibleAcropora cervicorniscoral genotypes (hereafter referred to simply as ‘genotypes’) before and after high temperature‐mediated bleaching. We found that the intracellular bacterial parasite ‘Ca.Aquarickettsia rohweri’ was strikingly abundant in disease‐susceptible genotypes. Disease‐resistant genotypes, however, had notably more diverse and even communities, with correspondingly low abundances of ‘Ca.Aquarickettsia’.Bleaching caused a dramatic reduction of ‘Ca.Aquarickettsia’ within disease‐susceptible corals and led to an increase in bacterial community dispersion, as well as the proliferation of opportunists. Our data support the hypothesis that ‘Ca.Aquarickettsia’ species increase coral disease risk through two mechanisms: (i) the creation of host nutritional deficiencies leading to a compromised host‐symbiont state and (ii) the opening of niche space for potential pathogens during thermal stress.more » « less
-
Abstract In root nodule symbioses (RNS) between nitrogen (N)‐fixing bacteria and plants, bacterial symbionts cycle between nodule‐inhabiting and soil‐inhabiting niches that exert differential selection pressures on bacterial traits. Little is known about how the resulting evolutionary tension between host plants and symbiotic bacteria structures naturally occurring bacterial assemblages in soils. We used DNA cloning to examine soil‐dwelling assemblages of the actinorhizal symbiontFrankiain sites with long‐term stable assemblages inAlnus incanassp.tenuifolianodules. We compared: (1) phylogenetic diversity ofFrankiain soil versus nodules, (2) change inFrankiaassemblages in soil versus nodules in response to environmental variation: both across succession, and in response to long‐term fertilization with N and phosphorus, and (3) soil assemblages in the presence and absence of host plants. Phylogenetic diversity was much greater in soil‐dwelling than nodule‐dwelling assemblages and fell into two large clades not previously observed. The presence of host plants was associated with enhanced representation of genotypes specific toA. tenuifolia, and decreased representation of genotypes specific to a secondAlnusspecies. The relative proportion of symbiotic sequence groups across a primary chronosequence was similar in both soil and nodule assemblages. Contrary to expectations, both N and P enhanced symbiotic genotypes relative to non‐symbiotic ones. Our results provide a rare set of field observations against which predictions from theoretical and experimental work in the evolutionary ecology of RNS can be compared.more » « less
-
Bonamia(Haplosporida) are oyster parasites capable of devastating oyster populations. The near-circumglobal distribution of the host generalistB. exitiosahas previously been associated with the natural and anthropogenic dispersal of broadly distributed non-commercial oysters in theOstrea stentinaspecies complex. Here, we took a global snapshot approach to explore the role of the widely introduced Pacific oysterMagallana gigas, a commercially important species that can be found on every continent except Antarctica, in transportingBonamia.We screened 938M. gigasindividuals from 41 populations in this oyster’s native and non-native geographic range for presence ofBonamiaDNA using PCR.B. exitiosawas the only species detected and only within 2 of 5 populations from southern California, USA (10 and 42% PCR prevalence). Therefore,M. gigascould have played a role in transportingB. exitiosato California (if introduced) and/or maintainingB. exitiosapopulations within California, but morphological confirmation of infection needs to be done to better understand the host-parasite dynamics within this system. We detected noBonamiaDNA within any other non-nativeM. gigaspopulations (n = 302) nor within nativeM. gigaspopulations in Japan and Korea (n = 582) and thus found no evidence to support the co-dispersal ofM. gigasand otherBonamiaspecies. Lower sample sizes within some populations and the non-systematic nature of our sampling design may have led to false negatives, especially in areas whereBonamiaare known to occur. Nevertheless, this global snapshot provides preliminary guidance for managing both natural and farmed oyster populations.more » « less
An official website of the United States government
