scholarly journals Major host transitions are modulated through transcriptome-wide reprograming events in Schistocephalus solidus, a threespine stickleback parasite

2016 ◽  
Author(s):  
François Olivier Hébert ◽  
Stephan Grambauer ◽  
Iain Barber ◽  
Christian R Landry ◽  
Nadia Aubin-Horth

ABSTRACTParasites with complex life cycles have developed numerous phenotypic strategies, closely associated with developmental events, to enable the exploitation of different ecological niches and facilitate transmission between hosts. How these environmental shifts are regulated from a metabolic and physiological standpoint, however, still remain to be fully elucidated. We examined the transcriptomic response of Schistocephalus solidus, a trophically-transmitted parasite with a complex life cycle, over the course of its development in an intermediate host, the threespine stickleback, and the final avian host. Results from our differential gene expression analysis show major reprogramming events among developmental stages. The final host stage is characterized by a strong activation of reproductive pathways and redox homeostasis. The attainment of infectivity in the fish intermediate host – which precedes sexual maturation in the final host and is associated with host behaviour changes – is marked by transcription of genes involved in neural pathways and sensory perception. Our results suggest that un-annotated and S. solidus-specific genes could play a determinant role in host-parasite molecular interactions required to complete the parasite’s life cycle. Our results permit future comparative analyses to help disentangle species-specific patterns of infection from conserved mechanisms, ultimately leading to a better understanding of the molecular control and evolution of complex life cycles.

2021 ◽  
Vol 288 (1964) ◽  
Author(s):  
Molly A. Albecker ◽  
Laetitia G. E. Wilkins ◽  
Stacy A. Krueger-Hadfield ◽  
Samuel M. Bashevkin ◽  
Matthew W. Hahn ◽  
...  

Complex life cycles, in which discrete life stages of the same organism differ in form or function and often occupy different ecological niches, are common in nature. Because stages share the same genome, selective effects on one stage may have cascading consequences through the entire life cycle. Theoretical and empirical studies have not yet generated clear predictions about how life cycle complexity will influence patterns of adaptation in response to rapidly changing environments or tested theoretical predictions for fitness trade-offs (or lack thereof) across life stages. We discuss complex life cycle evolution and outline three hypotheses—ontogenetic decoupling, antagonistic ontogenetic pleiotropy and synergistic ontogenetic pleiotropy—for how selection may operate on organisms with complex life cycles. We suggest a within-generation experimental design that promises significant insight into composite selection across life cycle stages. As part of this design, we conducted simulations to determine the power needed to detect selection across a life cycle using a population genetic framework. This analysis demonstrated that recently published studies reporting within-generation selection were underpowered to detect small allele frequency changes (approx. 0.1). The power analysis indicates challenging but attainable sampling requirements for many systems, though plants and marine invertebrates with high fecundity are excellent systems for exploring how organisms with complex life cycles may adapt to climate change.


Parasitology ◽  
2016 ◽  
Vol 143 (14) ◽  
pp. 1824-1846 ◽  
Author(s):  
DANIEL P. BENESH

SUMMARYComplex life cycles are common in free-living and parasitic organisms alike. The adaptive decoupling hypothesis postulates that separate life cycle stages have a degree of developmental and genetic autonomy, allowing them to be independently optimized for dissimilar, competing tasks. That is, complex life cycles evolved to facilitate functional specialization. Here, I review the connections between the different stages in parasite life cycles. I first examine evolutionary connections between life stages, such as the genetic coupling of parasite performance in consecutive hosts, the interspecific correlations between traits expressed in different hosts, and the developmental and functional obstacles to stage loss. Then, I evaluate how environmental factors link life stages through carryover effects, where stressful larval conditions impact parasites even after transmission to a new host. There is evidence for both autonomy and integration across stages, so the relevant question becomes how integrated are parasite life cycles and through what mechanisms? By highlighting how genetics, development, selection and the environment can lead to interdependencies among successive life stages, I wish to promote a holistic approach to studying complex life cycle parasites and emphasize that what happens in one stage is potentially highly relevant for later stages.


2010 ◽  
Vol 365 (1540) ◽  
pp. 631-640 ◽  
Author(s):  
Alessandro Minelli ◽  
Giuseppe Fusco

Metazoan life cycles can be complex in different ways. A number of diverse phenotypes and reproductive events can sequentially occur along the cycle, and at certain stages a variety of developmental and reproductive options can be available to the animal, the choice among which depends on a combination of organismal and environmental conditions. We hypothesize that a diversity of phenotypes arranged in developmental sequence throughout an animal's life cycle may have evolved by genetic assimilation of alternative phenotypes originally triggered by environmental cues. This is supported by similarities between the developmental mechanisms mediating phenotype change and alternative phenotype determination during ontogeny and the common ecological condition that favour both forms of phenotypic variation. The comparison of transcription profiles from different developmental stages throughout a complex life cycle with those from alternative phenotypes in closely related polyphenic animals is expected to offer critical evidence upon which to evaluate our hypothesis.


1991 ◽  
Vol 123 (1) ◽  
pp. 23-40 ◽  
Author(s):  
H.V. Danks

AbstractThe structure and temporal control of insect life cycles can best be understood by viewing them as pathways along which various options (e.g. develop or enter diapause; grow rapidly or grow slowly) are chosen in response to environmental controls such as photoperiod and temperature. Simple life cycles include small numbers of such options. The combination of several successive simple elements, however, can produce remarkably complex life cycle patterns, which are more prevalent than most entomologists have recognized. The ways in which these simple elements contribute to life cycle pathways are outlined and illustrated schematically. Flow charts showing the successive decision points in the life cycle then are constructed for selected species. This approach confirms the different simple elements, and shows how they are used in combination to control seasonal life cycles in nature.


2019 ◽  
Author(s):  
Chloé Suzanne Berger ◽  
Nadia Aubin-Horth

ABSTRACTParasites with complex life cycles have been proposed to manipulate the behaviour of their intermediate hosts to increase the probability of reaching their final host. The cause of these drastic behavioural changes could be manipulation factors released by the parasite in its environment (the secretome), but this has rarely been assessed. We studied a non-cerebral parasite, the cestode Schistocephalus solidus, and its intermediate host, the threespine stickleback (Gasterosteus aculeatus), whose response to danger becomes significantly diminished when infected. These altered behaviours appear only during late infection, when the worm is ready to reproduce in its final avian host. Sympatric host-parasite pairs show higher infection success for parasites, suggesting that the secretome effects could differ for allopatric host-parasite pairs with independent evolutionary histories. We tested the effects of secretome exposure on behaviour by using secretions from the early and late infection of S. solidus and by injecting them in healthy sticklebacks from a sympatric and allopatric population. Contrary to our prediction, secretome from late infection worms did not result in more risky behaviours, but secretome from early infection resulted in more cautious hosts, only in fish from the allopatric population. Our results suggest that the secretome of Schistocephalus solidus contains molecules that can affect host behaviour, that the causes underlying the behavioural changes in infected sticklebacks are multifactorial, and that local adaptation between host-parasite pairs may extend to the response to the parasite’s secretome content.


2009 ◽  
Vol 46 (1) ◽  
pp. 21-27 ◽  
Author(s):  
F. Lefebvre ◽  
B. Georgiev ◽  
R. Bray ◽  
D. Littlewood

AbstractThe Cestode Life Cycle Database (CLCdb) project was initiated in 2005 with the objective to develop a comprehensive and centralised resource to store, retrieve and analyse key information concerning tapeworm life cycles; e.g. morphogenesis, intermediate host identities, transmission patterns, etc. It constitutes the first electronic database to deal with complex life cycle information for any helminth taxon. Here we critically evaluate our experience after exhaustively entering data for our model group, the cyclophyllidean family Hymenolepididae. After providing basic statistics (530 consulted references; ∼ 230 ‘known’ life cycle), we identify future needs in turning the CLCdb into an open access monograph covering all cestode groups. We review the added benefits and potential utilities of the database for cestodologists and other users, including ecologists and veterinarians, and we call for specialist contributions. Since late 2007, a short version of the CLCdb has been available online, with basic functionalities and tools (www.nhm.ac.uk/research-curation/projects/cestode-life-cycle/index.html).


2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Ewa Pyrka ◽  
Gerard Kanarek ◽  
Grzegorz Zaleśny ◽  
Joanna Hildebrand

Abstract Background Leeches (Hirudinida) play a significant role as intermediate hosts in the circulation of trematodes in the aquatic environment. However, species richness and the molecular diversity and phylogeny of larval stages of strigeid trematodes (tetracotyle) occurring in this group of aquatic invertebrates remain poorly understood. Here, we report our use of recently obtained sequences of several molecular markers to analyse some aspects of the ecology, taxonomy and phylogeny of the genera Australapatemon and Cotylurus, which utilise leeches as intermediate hosts. Methods From April 2017 to September 2018, 153 leeches were collected from several sampling stations in small rivers with slow-flowing waters and related drainage canals located in three regions of Poland. The distinctive forms of tetracotyle metacercariae collected from leeches supplemented with adult Strigeidae specimens sampled from a wide range of water birds were analysed using the 28S rDNA partial gene, the second internal transcribed spacer region (ITS2) region and the cytochrome c oxidase (COI) fragment. Results Among investigated leeches, metacercariae of the tetracotyle type were detected in the parenchyma and musculature of 62 specimens (prevalence 40.5%) with a mean intensity reaching 19.9 individuals. The taxonomic generic affiliation of metacercariae derived from the leeches revealed the occurrence of two strigeid genera: Australapatemon Sudarikov, 1959 and Cotylurus Szidat, 1928. Phylogenetic reconstructions based on the partial 28S rRNA gene, ITS2 region and partial COI gene confirmed the separation of the Australapatemon and Cotylurus clades. Taking currently available molecular data and our results into consideration, recently sequenced tetracotyle of Australapatemon represents most probably Au. minor; however, unclear phylogenetic relationships between Au. burti and Au. minor reduce the reliability of this conclusion. On the other hand, on the basis of the obtained sequences, supplemented with previously published data, the metacercariae of Cotylurus detected in leeches were identified as two species: C. strigeoides Dubois, 1958 and C. syrius Dubois, 1934. This is the first record of C. syrius from the intermediate host. Conclusions The results of this study suggest the separation of ecological niches and life cycles between C. cornutus (Rudolphi, 1808) and C. strigeoides/C. syrius, with potential serious evolutionary consequences for a wide range of host–parasite relationships. Moreover, phylogenetic analyses corroborated the polyphyletic character of C. syrius, the unclear status of C. cornutus and the separate position of Cotylurus raabei Bezubik, 1958 within Cotylurus. The data demonstrate the inconsistent taxonomic status of the sequenced tetracotyle of Australapatemon, resulting, in our opinion, from the limited availability of fully reliable, comparative sequences of related taxa in GenBank.


1968 ◽  
Vol 42 (3-4) ◽  
pp. 295-298 ◽  
Author(s):  
J. M. Hamilton ◽  
A. W. McCaw

Aelurostrongylus abstrusus, the lungworm of the cat, has a world wide distribution and has been reported from countries as far apart as America, Great Britain and Palestine. It has a complex life cycle insofar as a molluscan intermediate host is essential and it is possible that auxiliary hosts also play an important part. In Britain, the incidence of active infestation of cats with the parasite has been recorded as 19·4% (Lewis, 1927) and 6·6% (Hamilton, 1966) but the latter author found that, generally, the clinical disease produced by the parasite was of a mild nature. It is known that the average patent period of the infestation in the cat is 8–13 weeks and it seems likely that, in that time, a considerable number of first stage larvae would be evacuated. Information on that point is not available and the object of the following experiment was to ascertain the number of larvae produced by cats during the course of a typical infestation.


Author(s):  
Jan A. Pechenik

I have a Hardin cartoon on my office door. It shows a series of animals thinking about the meaning of life. In sequence, we see a lobe-finned fish, a salamander, a lizard, and a monkey, all thinking, “Eat, survive, reproduce; eat, survive, reproduce.” Then comes man: “What's it all about?” he wonders. Organisms live to reproduce. The ultimate selective pressure on any organism is to survive long enough and well enough to pass genetic material to a next generation that will also be successful in reproducing. In this sense, then, every morphological, physiological, biochemical, or behavioral adaptation contributes to reproductive success, making the field of life cycle evolution a very broad one indeed. Key components include mode of sexuality, age and size at first reproduction (Roff, this volume), number of reproductive episodes in a lifetime, offspring size (Messina and Fox, this volume), fecundity, the extent to which parents protect their offspring and how that protection is achieved, source of nutrition during development, survival to maturity, the consequences of shifts in any of these components, and the underlying mechanisms responsible for such shifts. Many of these issues are dealt with in other chapters. Here I focus exclusively on animals, and on a particularly widespread sort of life cycle that includes at least two ecologically distinct free-living stages. Such “complex life cycles” (Istock 1967) are especially common among amphibians and fishes (Hall and Wake 1999), and within most invertebrate groups, including insects (Gilbert and Frieden 1981), crustaceans, bivalves, gastropods, polychaete worms, echinoderms, bryozoans, and corals and other cnidarians (Thorson 1950). In such life cycles, the juvenile or adult stage is reached by metamorphosing from a preceding, free-living larval stage. In many species, metamorphosis involves a veritable revolution in morphology, ecology, behavior, and physiology, sometimes taking place in as little as a few minutes or a few hours. In addition to the issues already mentioned, key components of such complex life cycles include the timing of metamorphosis (i.e., when it occurs), the size at which larvae metamorphose, and the consequences of metamorphosing at particular times or at particular sizes. The potential advantages of including larval stages in the life history have been much discussed.


Parasitology ◽  
2011 ◽  
Vol 138 (9) ◽  
pp. 1183-1192 ◽  
Author(s):  
KRISTIN K. HERRMANN ◽  
ROBERT POULIN

SUMMARYEach transmission event in complex, multi-host life cycles create obstacles selecting for adaptations by trematodes. One such adaptation is life cycle abbreviation through progenesis, in which the trematode precociously matures and reproduces within the second intermediate host. Progenesis eliminates the need for the definitive host and increases the chance of life cycle completion. However, progenetic individuals face egg-dispersal challenges associated with reproducing within metacercarial cysts in the tissues or body cavity of the second intermediate host. Most progenetic species await host death for their eggs to be released into the environment. The present study investigated temporal variation of progenesis in Stegodexamene anguillae in one of its second intermediate fish hosts and the effect of the fish's reproductive cycle on progenesis. The study involved monthly sampling over 13 months at one locality. A greater proportion of individuals became progenetic in the gonads of female fish hosts. Additionally, progenesis of worms in the gonads was correlated with seasonal daylight and temperature changes, major factors controlling fish reproduction. Host spawning events are likely to be an avenue of egg dispersal for this progenetic species, with the adoption of progenesis being conditional on whether or not the parasite can benefit from fish spawning.


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