Life-cycle complexity in helminths Benesh, Daniel P.; Parker, Geoff; Chubb, James C.
Evolution,
08/2021, Letnik:
75, Številka:
8
Journal Article
Recenzirano
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Parasitic worms (i.e., helminths) commonly infect multiple hosts in succession. With every transmission step, they risk not infecting the next host and thus dying before reproducing. Given this risk, ...what are the benefits of complex life cycles? Using a dataset for 973 species of trophically transmitted acanthocephalans, cestodes, and nematodes, we tested whether hosts at the start of a life cycle increase transmission and whether hosts at the end of a life cycle enable growth to larger, more fecund sizes. Helminths with longer life cycles, that is, more successive hosts, infected conspicuously smaller first hosts, slightly larger final hosts, and exploited trophic links with lower predator–prey mass ratios. Smaller first hosts likely facilitate transmission because of their higher abundance and because parasite propagules were the size of their normal food. Bigger definitive hosts likely increase fecundity because parasites grew larger in big hosts, particularly endotherms. Helminths with long life cycles attained larger adult sizes through later maturation, not faster growth. Our results indicate that complex helminth life cycles are ubiquitous because growth and reproduction are highest in large, endothermic hosts that are typically only accessible via small intermediate hosts, that is, the best hosts for growth and transmission are not the same.
Parasitic worms (helminths) with complex life cycles divide growth and development between successive hosts. Using data from 597 species of acanthocephalans, cestodes, and nematodes with two‐host ...life cycles, we found that helminths with larger intermediate hosts were more likely to infect larger, endothermic definitive hosts, although some evolutionary shifts in definitive host mass occurred without changes in intermediate host mass. Life‐history theory predicts parasites to shift growth to hosts in which they can grow rapidly and/or safely. Accordingly, helminth species grew relatively less as larvae and more as adults if they infected smaller intermediate hosts and/or larger, endothermic definitive hosts. Growing larger than expected in one host, relative to host mass/endothermy, was not associated with growing less in the other host, implying a lack of cross‐host trade‐offs. Rather, some helminth orders had both large larvae and large adults. Within these taxa, however, size at maturity in the definitive host was unaffected by changes to larval growth, as predicted by optimality models. Parasite life‐history strategies were mostly (though not entirely) consistent with theoretical expectations, suggesting that helminths adaptively divide growth and development between the multiple hosts in their complex life cycles.
BACKGROUND:Reports of more than two cutaneous perforator angiosome territories being raised successfully in distally based sural flaps are appearing in the literature. Previous anatomical studies ...have noted that cutaneous arteries, connected by true anastomosis without change in caliber, frequently parallel cutaneous nerves.
METHODS:Twenty-four (48 sides) total body lead oxide cadaver injection studies, including seven arterial and two venous neurovascular, were examined, and the results were compared with clinical thermography in Part II.
RESULTS:Long branches of cutaneous perforators, connected in a series by true anastomoses, paralleled at variable distances the main trunks of cutaneous nerves in the head, neck, torso, and upper and lower extremities. Specifically, in the leg, an average of 3.2 true anastomoses (range, 1 to 5) connected perforators that paralleled the sural nerve on the back of the calf; and 2.5 (range, 1 to 4) connected perforators on the medial side of the leg. These vascular freeways were paralleled by the short and long saphenous veins, respectively.
CONCLUSIONS:True anastomoses frequently connect skin perforators that course in parallel with cutaneous nerves and veins. They provide an explanation for the long viable flaps noted in the leg, and it will be shown in Part II that they can be detected preoperatively with thermography.
BACKGROUND:Cadaveric studies have revealed that cutaneous perforators are linked by either reduced-caliber “choke” arteries, or by vessels without change in caliber, the true anastomoses. These true ...anastomotic vessels are often found in parallel with the cutaneous nerves and accompanying veins, and are associated both experimentally and clinically with larger areas of flap survival. The Doppler probe and computed tomographic angiography are already used preoperatively to determine perforator locations but currently cannot reveal the type of anastomotic connections.
METHODS:Thermal images were taken in a previously described fashion and compared with both computed tomographic angiographic studies where available and with cadaveric angiographic studies previously performed by the authors’ laboratory.
RESULTS:Perforators larger than 1 mm were accurately localized by thermography when compared with computed tomographic angiography. Perforator angiosome rewarming closely approximated a log-based line of best fit. Interperforator zones were variable in their rewarming and correlated with known anatomical patterns of true and choke anastomoses between perforator angiosomes.
CONCLUSIONS:Thermography now offers a new modality with which to bridge the gap not only by identifying the perforator “hot spots” but also by the robustness of their interconnections. The pattern of these interconnections seen on thermographic imaging has in turn been found to match those seen in the authors’ cadaveric studies.
Parasitic worms with complex life cycles have several developmental stages, with each stage creating opportunities to infect additional host species. Using a data set for 973 species of trophically ...transmitted acanthocephalans, cestodes, and nematodes, we confirmed that worms with longer life cycles (i.e., more successive hosts) infect a greater diversity of host species and taxa (after controlling for study effort). Generalism at the stage level was highest for middle life stages, the second and third intermediate hosts of long life cycles. By simulating life cycles in real food webs, we found that middle stages had more potential host species to infect, suggesting that opportunity constrains generalism. However, parasites usually infected fewer host species than expected from simulated cycles, suggesting that generalism has costs. There was no trade-off in generalism from one stage to the next, but worms spent less time growing and developing in stages where they infected more taxonomically diverse hosts. Our results demonstrate that life-cycle complexity favors high generalism and that host use across life stages is determined by both ecological opportunity and life-history trade-offs.
Parasitic worms (helminths) frequently have complex life cycles in which they are transmitted trophically between two or more successive hosts. Sexual reproduction often takes place in high ...trophic-level (TL) vertebrates, where parasites can grow to large sizes with high fecundity. Direct infection of high TL hosts, while advantageous, may be unachievable for parasites constrained to transmit trophically, because helminth propagules are unlikely to be ingested by large predators. Lack of niche overlap between propagule and definitive host (the trophic transmission vacuum) may explain the origin and/or maintenance of intermediate hosts, which overcome this transmission barrier. We show that nematodes infecting high TL definitive hosts tend to have more successive hosts in their life cycles. This relationship was modest, though, driven mainly by the minimum TL of hosts, suggesting that the shortest trophic chains leading to a host define the boundaries of the transmission vacuum. We also show that alternative modes of transmission, like host penetration, allow nematodes to reach high TLs without intermediate hosts. We suggest that widespread omnivory as well as parasite adaptations to increase transmission probably reduce, but do not eliminate, the barriers to the transmission of helminths through the food web.
Why do so many parasitic worms have complex life-cycles? A complex life-cycle has at least two hypothesized costs: (i) worms with longer life-cycles, i.e. more successive hosts, must be generalists ...at the species level, which might reduce lifetime survival or growth, and (ii) each required host transition adds to the risk that a worm will fail to complete its life-cycle. Comparing hundreds of trophically transmitted acanthocephalan, cestode, and nematode species with different life-cycles suggests these costs are weaker than expected. Helminths with longer cycles exhibit higher species-level generalism without impaired lifetime growth. Further, risk in complex life-cycles is mitigated by increasing establishment rates in each successive host. Two benefits of longer cycles are transmission and production. Longer cycles normally include smaller (and thus more abundant) first hosts that are likely to consume parasite propagules, as well as bigger (and longer-lived) definitive hosts, in which adult worms grow to larger and presumably more fecund reproductive sizes. Additional factors, like host immunity or dispersal, may also play a role, but are harder to address. Given the ubiquity of complex life-cycles, the benefits of incorporating or retaining hosts in a cycle must often exceed the costs.
Display omitted
•Comparing helminth species hints at the costs and benefits of complex life-cycles.•Generalism and survival costs in longer life-cycles are weaker than expected.•Longer life-cycles have growth and transmission benefits.•The benefits of a complex life-cycle must often exceed the costs.
Background
Mesenchymal stromal cells (MSCs) have been shown in rodent models to promote primary and pulmonary metastatic sarcoma growth when injected in the presence of gross tumor. In theory, this ...would limit their use in a clinical setting after limb salvage treatment for osteosarcoma. Although concerning, these models do not translate to the clinical setting wherein MSCs could be used after primary tumor resection to aid in bone healing and incorporation of tumor endoprostheses. If we can determine whether the use of MSCs in this setting is safe, it might improve our ability to augment bone healing in patients undergoing limb salvage.
Questions/purposes
The purpose of this study was to determine (1) whether MSCs promote pulmonary metastatic disease progression in a murine osteosarcoma model; and/or (2) whether they affect local disease recurrence in the presence of microscopic residual osteosarcoma.
Methods
An orthotopic model of luciferase-expressing osteosarcoma was developed. At 10 days, resection of the primary tumor was performed. One hundred fourteen female C3H mice were inoculated with DLM8-luc osteosarcoma in the proximal tibia. Ninety-four mice developed orthotopic osteosarcoma with luciferase expression. Mice with bioluminescent evidence of a primary tumor received either a microscopically “clean” amputation at a time when residual microscopic metastatic disease was present in the lungs (pulmonary metastasis group; n = 65) or a “dirty” amputation (local recurrence group; n = 29). Mice were randomized to receive intravenous MSCs, MSCs at the surgical site, or no MSCs. Mice were monitored for development and progression of pulmonary metastasis and local recurrence by bioluminescence imaging and daily measurements at the surgical site. The number of pulmonary nodules, time to first evidence of metastasis, and size of recurrent tumor were compared using Kruskal-Wallis, analysis of variance, Welch’s, t-tests, or Mann-Whitney tests as appropriate for the specific data sets with p < 0.05 considered significant.
Results
Mice receiving intravenous MSCs had a faster time to first detection of pulmonary metastasis (2.93 ± 1.90 days) compared with mice with local injection of MSCs (6.94 ± 6.78 days) or no MSCs (5.93 ± 4.55 days) (p = 0.022). MSC treatment did not influence whether mice developed local recurrence (p = 0.749) or size of recurrent tumors (p = 0.221).
Conclusions
MSCs delivered to the surgical site did not promote local recurrence or size of recurrent tumors, but intravenous injection of MSCs did hasten onset of detection of pulmonary metastatic disease. Although local administration of MSCs into a surgical site does not appear to promote either pulmonary metastatic disease or local recurrence, large variation within groups and small numbers diminished statistical power such that a Type II error cannot be ruled out.
Clinical Relevance
If MSCs are to be used to augment bone healing in the postlimb salvage setting in patients with osteosarcoma, it will be important to understand their influence, if any, on pulmonary micrometastsis or residual microscopic local disease. Although murine models do not completely recapitulate the clinical scenario, these results suggest that intravenous delivery of MSCs may promote micrometastatic pulmonary disease. Local administration into a surgical wound, even in the presence of residual microscopic disease, may be safe, at least in this murine model, but further investigation is warranted before considering the use of MSCs for clinical use in patients with osteosarcoma.
Organisms with complex life cycles occupy distinct niches as larvae and adults. One presumed advantage of this is the ability to exploit different resources successively throughout ontogeny. Various ...taxa, however, have evolved nonfeeding, nongrowing adult stages. We show theoretically that this counterintuitive no-growth strategy is favored when the optimal larval size is greater than or equal to the optimal adult size for reproduction. We empirically investigated this in a group of parasitic worms (helminths). Helminths are transmitted trophically between hosts before reproducing in large, high-trophic-level hosts, and most undergo considerable growth as adults in their final host. Some well-studied tapeworm species (Schistocephalus,Ligula, andDigrammaspecies) are notable exceptions; they reproduce semelparously without any growth in their final habitat (the gut of piscivorous birds). Using cross-species comparative analyses, we show that these tapeworms that do not grow in their final host (1) attain larval sizes in their last intermediate host (fishes) that are comparable to or larger than the adult sizes reached by tapeworms that do grow in the same adult niche (also piscivorous birds) and (2) are large, even as larvae, relative to the mass of their final hosts. These results are consistent with the idea that a massive larval size can make adult growth superfluous, and we discuss whether this likely applies to other complex life cycle taxa with nonfeeding, nongrowing adults.
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