Title: Co-infesting symbionts on a threatened marine host: evaluating correlations between an introduced parasitic isopod and a native symbiotic clam
In marine ecosystems, increased global-scale transportation creates opportunities for rapid introduction of invasive parasitic species that, in some cases, result in dramatic shifts within the native communities. A lack of detailed knowledge regarding the ecology of invasive marine parasites hinders our ability to develop effective conservation strategies and avoid unforeseen ecological consequences. We examined co-infestation patterns of a highly pathogenic, introduced parasitic isopod (Orthione griffenis) and a native symbiotic clam (Neaeromya rugifera) on the North American native blue mud shrimp Upogebia pugettensis. Our comparisons included infestations of O. griffenis and N. rugifera among 447 U. pugettensis hosts over 3 study years and were designed to statistically assess whether the 2 symbionts exhibited significant associations with one another. Our results indicate that infestations by the 2 symbiont species are positively correlated, such that the presence of one symbiont is a strong, positive predictor for the presence of the other. For both symbionts, host size is an important factor that drives the observed correlation. Host sex is also influential for O. griffenis. Interestingly, even after accounting for these host attributes, the infestations by the 2 symbionts continue to correlate positively, particularly among older (second-year and beyond) symbionts, highlighting the likely influence of additional host and environmental factors in driving the symbiont correlation post-settlement. We consider potential mechanisms, including differential energetic reserves and longevities between infested and co-infested hosts, in detail. These results offer insights into the ecological drivers of symbiont co-infestation, which have important implications for understanding host-parasite interactions and future conservation measures. more »« less
Many animals live in intimate associations with a species-rich microbiome. A key factor in maintaining these beneficial associations is fidelity, defined as the stability of associations between hosts and their microbiota over multiple host generations. Fidelity has been well studied in terrestrial hosts, particularly insects, over longer macroevolutionary time. In contrast, little is known about fidelity in marine animals with species-rich microbiomes at short microevolutionary time scales, that is at the level of a single host population. Given that natural selection acts most directly on local populations, studies of microevolutionary partner fidelity are important for revealing the ecological and evolutionary processes that drive intimate beneficial associations within animal species.
Results
In this study on the obligate symbiosis between the gutless marine annelidOlavius algarvensisand its consortium of seven co-occurring bacterial symbionts, we show that partner fidelity varies across symbiont species from strict to absent over short microevolutionary time. Using a low-coverage sequencing approach that has not yet been applied to microbial community analyses, we analysed the metagenomes of 80O. algarvensisindividuals from the Mediterranean and compared host mitochondrial and symbiont phylogenies based on single-nucleotide polymorphisms across genomes. Fidelity was highest for the two chemoautotrophic, sulphur-oxidizing symbionts that dominated the microbial consortium of allO. algarvensisindividuals. In contrast, fidelity was only intermediate to absent in the sulphate-reducing and spirochaetal symbionts with lower abundance. These differences in fidelity are likely driven by both selective and stochastic forces acting on the consistency with which symbionts are vertically transmitted.
Conclusions
We hypothesize that variable degrees of fidelity are advantageous forO. algarvensisby allowing the faithful transmission of their nutritionally most important symbionts and flexibility in the acquisition of other symbionts that promote ecological plasticity in the acquisition of environmental resources.
Wu, Qiang; Miles, Donald B.; Richard, Murielle; Rutschmann, Alexis; Clobert, Jean(
, Global Change Biology)
Abstract
Climate‐modulated parasitism is driven by a range of factors, yet the spatial and temporal variability of this relationship has received scant attention in wild vertebrate hosts. Moreover, most prior studies overlooked the intraspecific differences across host morphotypes, which impedes a full understanding of the climate–parasitism relationship. In the common lizard (Zootoca vivipara), females exhibit three colour morphs: yellow (Y‐females), orange (O‐females) and mixed (mixture of yellow and orange, M‐females).Zootoca viviparais also infested with an ectoparasite (Ophionyssusmites). We therefore used this model system to examine the intraspecific response of hosts to parasitism under climate change. We found infestation probability to differ across colour morphs at both spatial (10 sites) and temporal (20 years) scales: M‐females had lower parasite infestations than Y‐ and O‐females at lower temperatures, but became more susceptible to parasites as temperature increased. The advantage of M‐females at low temperatures was counterbalanced by their higher mortality rates thereafter, which suggests a morph‐dependent trade‐off between resistance to parasites and host survival. Furthermore, significant interactions between colour morphs and temperature indicate that the relationship between parasite infestations and climate warming was contingent on host morphotypes. Parasite infestations increased with temperature for most morphs, but displayed morph‐specific rates. Finally, infested M‐females had higher reductions in survival rates than infested Y‐ or O‐females, which implies a potential loss of intraspecific diversity within populations as parasitism and temperatures rise. Overall, we found parasitism increases with warming temperatures, but this relationship is modulated by host morphotypes and an interaction with temperature. We suggest that epidemiological models incorporate intraspecific diversity within species for better understanding the dynamics of wildlife diseases under climate warming.
McDermott, John J.; Williams, Jason D.; Boyko, Christopher B.(
, Journal of Crustacean Biology)
Abstract
Pinnixion sexdecennia n. gen., n. sp. is described from three pinnotherid hosts: Austinixa gorei (Manning & Felder, 1989), Pinnixa chaetopterana Stimpson, 1860, and Zaops ostreus (Say, 1817). Females of the new species are distinguished from all other entoniscids by possessing two transverse lobes on oostegite 1 and fused oostegites 2–5; males have a pair of lateral expansions on each of the first two pleomeres. The epicaridium larvae of the new species also have a unique elongated, cylindrical terminal process on the pereopod 6 dactylus. Pinnixion sexdecennian. gen., n. sp. exhibited highest prevalence (> 40%) in North Carolina and Florida. Examination of live specimens of P. chaetopterana infested with mature female isopods showed that larvae are liberated via a pore produced in the wall of the host’s branchial chamber. Mature females of P. sexdecennian. gen., n. sp. occupied nearly all available space within the host crab’s hemocoel. Female P. chaetopterana had higher prevalence than males, and intensities of infestations were also greater in females. Evidence from all locations showed that mature parasites do not inhibit breeding or molting in the host. Our report is one of the few studies on the ecology and biology of entoniscids, a cryptic but ecologically important group of parasitic isopods. We also resolve long-standing nomenclatural issues involving Entione Kossmann, 1881 and Entioninae Codreanu, Codreanu & Pike, 1960, the subfamily to which the new genus and species belongs, by synonymizing Grapsion Giard & Bonnier, 1886 with Entione.
Carpenter, Melissa; Peng, Linyao; Smith, Andrew H.; Joffe, Jonah; O’Connor, Michael; Oliver, Kerry M.; Russell, Jacob A.(
, Insects)
Insects harbor a variety of maternally inherited bacterial symbionts. As such, variation in symbiont presence/absence, in the combinations of harbored symbionts, and in the genotypes of harbored symbiont species provide heritable genetic variation of potential use in the insects’ adaptive repertoires. Understanding the natural importance of symbionts is challenging but studying their dynamics over time can help to elucidate the potential for such symbiont-driven insect adaptation. Toward this end, we studied the seasonal dynamics of six maternally transferred bacterial symbiont species in the multivoltine pea aphid (Acyrthosiphon pisum). Our sampling focused on six alfalfa fields in southeastern Pennsylvania, and spanned 14 timepoints within the 2012 growing season, in addition to two overwintering periods. To test and generate hypotheses on the natural relevance of these non-essential symbionts, we examined whether symbiont dynamics correlated with any of ten measured environmental variables from the 2012 growing season, including some of known importance in the lab. We found that five symbionts changed prevalence across one or both overwintering periods, and that the same five species underwent such frequency shifts across the 2012 growing season. Intriguingly, the frequencies of these dynamic symbionts showed robust correlations with a subset of our measured environmental variables. Several of these trends supported the natural relevance of lab-discovered symbiont roles, including anti-pathogen defense. For a seventh symbiont—Hamiltonella defensa—studied previously across the same study periods, we tested whether a reported correlation between prevalence and temperature stemmed not from thermally varying host-level fitness effects, but from selection on co-infecting symbionts or on aphid-encoded alleles associated with this bacterium. In general, such “hitchhiking” effects were not evident during times with strongly correlated Hamiltonella and temperature shifts. However, we did identify at least one time period in which Hamiltonella spread was likely driven by selection on a co-infecting symbiont—Rickettsiella viridis. Recognizing the broader potential for such hitchhiking, we explored selection on co-infecting symbionts as a possible driver behind the dynamics of the remaining six species. Out of twelve examined instances of symbiont dynamics unfolding across 2-week periods or overwintering spans, we found eight in which the focal symbiont underwent parallel frequency shifts under single infection and one or more co-infection contexts. This supported the idea that phenotypic variation created by the presence/absence of individual symbionts is a direct target for selection, and that symbiont effects can be robust under co-habitation with other symbionts. Contrastingly, in two cases, we found that selection may target phenotypes emerging from symbiont co-infections, with specific species combinations driving overall trends for the focal dynamic symbionts, without correlated change under single infection. Finally, in three cases—including the one described above for Hamiltonella—our data suggested that incidental co-infection with a (dis)favored symbiont could lead to large frequency shifts for “passenger” symbionts, conferring no apparent cost or benefit. Such hitchhiking has rarely been studied in heritable symbiont systems. We propose that it is more common than appreciated, given the widespread nature of maternally inherited bacteria, and the frequency of multi-species symbiotic communities across insects.
Stoy, Kayla S.; Chavez, Joselyne; De Las Casas, Valeria; Talla, Venkat; Berasategui, Aileen; Morran, Levi T.; Gerardo, Nicole M.(
, Evolution)
Abstract
Many interspecific interactions are shaped by coevolution. Transmission mode is thought to influence opportunities for coevolution within symbiotic interactions. Vertical transmission maintains partner fidelity, increasing opportunities for coevolution, but horizontal transmission may disrupt partner fidelity, potentially reducing opportunities for coevolution. Despite these predictions, the role of coevolution in the maintenance of horizontally transmitted symbioses is unclear. Leveraging a tractable insect–bacteria symbiosis, we tested for signatures of pairwise coevolution by assessing patterns of host–symbiont specialization. If pairwise coevolution defines the interaction, we expected to observe evidence of reciprocal specialization between hosts and their local symbionts. We found no evidence for local adaptation between sympatric lineages of Anasa tristis squash bugs and Caballeronia spp. symbionts across their native geographic range. We also found no evidence for specialization between three co-localized Anasa host species and their native Caballeronia symbionts. Our results demonstrate generalist dynamics underlie the interaction between Anasa insect hosts and their Caballeronia symbionts. We predict that selection from multiple host species may favor generalist symbiont traits through diffuse coevolution. Alternatively, selection for generalist traits may be a consequence of selection by hosts for fixed cooperative symbiont traits without coevolution.
Li, J., Chapman, J., and Johnson, P. Co-infesting symbionts on a threatened marine host: evaluating correlations between an introduced parasitic isopod and a native symbiotic clam. Retrieved from https://par.nsf.gov/biblio/10353333. Marine ecology . Web. doi:10.3354/meps14105.
Li, J., Chapman, J., & Johnson, P. Co-infesting symbionts on a threatened marine host: evaluating correlations between an introduced parasitic isopod and a native symbiotic clam. Marine ecology, (). Retrieved from https://par.nsf.gov/biblio/10353333. https://doi.org/10.3354/meps14105
Li, J., Chapman, J., and Johnson, P.
"Co-infesting symbionts on a threatened marine host: evaluating correlations between an introduced parasitic isopod and a native symbiotic clam". Marine ecology (). Country unknown/Code not available. https://doi.org/10.3354/meps14105.https://par.nsf.gov/biblio/10353333.
@article{osti_10353333,
place = {Country unknown/Code not available},
title = {Co-infesting symbionts on a threatened marine host: evaluating correlations between an introduced parasitic isopod and a native symbiotic clam},
url = {https://par.nsf.gov/biblio/10353333},
DOI = {10.3354/meps14105},
abstractNote = {In marine ecosystems, increased global-scale transportation creates opportunities for rapid introduction of invasive parasitic species that, in some cases, result in dramatic shifts within the native communities. A lack of detailed knowledge regarding the ecology of invasive marine parasites hinders our ability to develop effective conservation strategies and avoid unforeseen ecological consequences. We examined co-infestation patterns of a highly pathogenic, introduced parasitic isopod (Orthione griffenis) and a native symbiotic clam (Neaeromya rugifera) on the North American native blue mud shrimp Upogebia pugettensis. Our comparisons included infestations of O. griffenis and N. rugifera among 447 U. pugettensis hosts over 3 study years and were designed to statistically assess whether the 2 symbionts exhibited significant associations with one another. Our results indicate that infestations by the 2 symbiont species are positively correlated, such that the presence of one symbiont is a strong, positive predictor for the presence of the other. For both symbionts, host size is an important factor that drives the observed correlation. Host sex is also influential for O. griffenis. Interestingly, even after accounting for these host attributes, the infestations by the 2 symbionts continue to correlate positively, particularly among older (second-year and beyond) symbionts, highlighting the likely influence of additional host and environmental factors in driving the symbiont correlation post-settlement. We consider potential mechanisms, including differential energetic reserves and longevities between infested and co-infested hosts, in detail. These results offer insights into the ecological drivers of symbiont co-infestation, which have important implications for understanding host-parasite interactions and future conservation measures.},
journal = {Marine ecology},
author = {Li, J. and Chapman, J. and Johnson, P.},
}
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