scholarly journals Experimental evolution of parasitic host manipulation

2019 ◽  
Vol 286 (1895) ◽  
pp. 20182413 ◽  
Author(s):  
Nina Hafer-Hahmann
Keyword(s):  
Experimental Evolution ◽  
Fish Host ◽  
Host Manipulation ◽  
Extended Phenotype ◽  
Parasite Fitness ◽  
Three Generations ◽  
Schistocephalus Solidus ◽  
Trade Offs

Host manipulation is a parasite-induced alteration of a host's phenotype that increases parasite fitness. However, if genetically encoded in the parasite, it should be under selection in the parasite. Such host manipulation has often been assumed to be energetically costly, which should restrict its evolution. Evidence of such costs, however, remains elusive. The trophically transmitted cestode Schistocephalus solidus manipulates the activity of its first intermediate copepod host to reduce its predation susceptibility before the parasite is ready for transmission. Thereafter, S. solidus increases host activity to facilitate transmission to its subsequent fish host. I selected S. solidus for or against host manipulation over three generations to investigate the evolvability of manipulation and identify potential trade-offs. Host manipulation responded to selection, confirming that this trait is heritable in the parasite and hence can present an extended phenotype. Changes in host manipulation were not restrained by any obvious costs.

scholarly journals The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions

2020 ◽  
Author(s):  
Chloé Suzanne Berger ◽  
Jérôme Laroche ◽  
Halim Maaroufi ◽  
Hélène Martin ◽  
Kyung-Mee Moon ◽  
...  
Keyword(s):  
Gasterosteus Aculeatus ◽  
Gene Prediction ◽  
Life Stage ◽  
Complex Mixture ◽  
Fish Host ◽  
Complex Life Cycle ◽  
Host Manipulation ◽  
Immune Functions ◽  
Phospholipid Scramblase ◽  
Schistocephalus Solidus

ABSTRACTManipulative parasites are predicted to liberate molecules in their external environment acting as manipulation factors with biological functions implicated in their host’s physiological and behavioural alterations. These manipulation factors are expected to be part of a complex mixture called the secretome. While the secretomes of various parasites have been described, there is very little data for a putative manipulative parasite. Here, we used proteomics to characterize the secretome of a model cestode with a complex life cycle based on trophic transmission. We studied Schistocephalus solidus during the life stage in which behavioural changes have been described in its obligatory intermediate fish host, the threespine stickleback (Gasterosteus aculeatus). We re-sequenced the genome of S. solidus using a combination of long and short reads to improve protein coding gene prediction and annotation for this parasite species. We then described the whole worm’s proteome and its secretome during fish host infection, using LC-MS/MS. A total of 2 290 proteins were detected in the proteome of S. solidus, with 30 proteins detected only in the secretome. We found that the secretome contained proteases, proteins with neural and immune functions, as well as proteins involved in cell communication. We also detected Receptor-type tyrosine-protein phosphatases, which were reported in other parasitic systems to be strong manipulation factors. The secretome also contained a Phospholipid scramblase that clustered phylogenetically with a stickleback Phospholipid scramblase, suggesting it could have the potential to interfere with the function of the scramblase in the host’s brain. Finally, we detected 12 S. solidus-specific proteins in the secretome that may play important roles in host-parasite interactions. Our results suggest that this parasite liberates molecules with putative host manipulation functions in the host and that many of them are species specific.

scholarly journals Inter- and intraspecific conflicts between parasites over host manipulation

2016 ◽  
Vol 283 (1824) ◽  
pp. 20152870 ◽  
Author(s):  
Nina Hafer ◽  
Manfred Milinski
Keyword(s):  
Intermediate Host ◽  
Fish Host ◽  
Host Manipulation ◽  
Schistocephalus Solidus ◽  
Common Strategy ◽  
First Intermediate Host

Host manipulation is a common strategy by which parasites alter the behaviour of their host to enhance their own fitness. In nature, hosts are usually infected by multiple parasites. This can result in a conflict over host manipulation. Studies of such a conflict in experimentally infected hosts are rare. The cestode Schistocephalus solidus (S) and the nematode Camallanus lacustris (C) use copepods as their first intermediate host. They need to grow for some time inside this host before they are infective and ready to be trophically transmitted to their subsequent fish host. Accordingly, not yet infective parasites manipulate to suppress predation. Infective ones manipulate to enhance predation. We experimentally infected laboratory-bred copepods in a manner that resulted in copepods harbouring (i) an infective C plus a not yet infective C or S, or (ii) an infective S plus a not yet infective C. An infective C completely sabotaged host manipulation by any not yet infective parasite. An infective S partially reduced host manipulation by a not yet infective C. We hence show experimentally that a parasite can reduce or even sabotage host manipulation exerted by a parasite from a different species.

scholarly journals Does resource availability affect host manipulation? – an experimental test with Schistocephalus solidus

2015 ◽  
Vol 1 ◽  
Author(s):  
NINA HAFER ◽  
DANIEL P. BENESH
Keyword(s):  
Resource Availability ◽  
Parasite Transmission ◽  
Host Manipulation ◽  
Food Treatment ◽  
Schistocephalus Solidus ◽  
Trade Offs ◽  
Common Strategy ◽  
Food Conditions ◽  
The Difference ◽  
Host Behaviour

SUMMARYHost manipulation is a common strategy of parasites employed to increase their fitness by changing the phenotype of their hosts. Whether host manipulation might be affected by environmental factors such as resource availability, has received little attention. We experimentally infected laboratory-bred copepods with the cestodeSchistocephalus solidus, submitted infected and uninfected copepods to either a high or a low food treatment, and measured their behaviour. Infection reduced host activity and speed in both feeding treatments. However, the difference between the infected and uninfected copepods was smaller under low food conditions, because uninfected, but not infected, copepods moved slower under these conditions. We suggest that these differences are mediated by the physical condition of copepods rather than changes in how strongly the parasite manipulated host behaviour. Additionally, we measured three fitness-relevant traits (growth, development and infection rate in the next host) of the parasite to identify potential trade-offs with host manipulation. The largest parasites in copepods appeared the least manipulative, i.e. their hosts showed the smallest behavioural alterations, but this may again reflect variation in copepod condition, rather than life history trade-offs between parasite growth and host manipulation. Our results point to the possibility that parasite transmission depends on environmental conditions.

scholarly journals The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions

2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Chloé Suzanne Berger ◽  
Jérôme Laroche ◽  
Halim Maaroufi ◽  
Hélène Martin ◽  
Kyung-Mee Moon ◽  
...  
Keyword(s):  
Gasterosteus Aculeatus ◽  
Gene Prediction ◽  
Life Stage ◽  
Cell Communication ◽  
Complex Mixture ◽  
Fish Host ◽  
Complex Life Cycle ◽  
Host Manipulation ◽  
Immune Functions ◽  
Schistocephalus Solidus

Abstract Background Manipulative parasites are thought to liberate molecules in their external environment, acting as manipulation factors with biological functions implicated in their host’s physiological and behavioural alterations. These manipulation factors are part of a complex mixture called the secretome. While the secretomes of various parasites have been described, there is very little data for a putative manipulative parasite. It is necessary to study the molecular interaction between a manipulative parasite and its host to better understand how such alterations evolve. Methods Here, we used proteomics to characterize the secretome of a model cestode with a complex life cycle based on trophic transmission. We studied Schistocephalus solidus during the life stage in which behavioural changes take place in its obligatory intermediate fish host, the threespine stickleback (Gasterosteus aculeatus). We produced a novel genome sequence and assembly of S. solidus to improve protein coding gene prediction and annotation for this parasite. We then described the whole worm’s proteome and its secretome during fish host infection using LC–MS/MS. Results A total of 2290 proteins were detected in the proteome of S. solidus, and 30 additional proteins were detected specifically in the secretome. We found that the secretome contains proteases, proteins with neural and immune functions, as well as proteins involved in cell communication. We detected receptor-type tyrosine-protein phosphatases, which were reported in other parasitic systems to be manipulation factors. We also detected 12 S. solidus-specific proteins in the secretome that may play important roles in host–parasite interactions. Conclusions Our results suggest that S. solidus liberates molecules with putative host manipulation functions in the host and that many of them are species-specific. Graphical abstract

scholarly journals Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

BMC Biology ◽  
2021 ◽  
Vol 19 (1) ◽  
Author(s):  
Basabi Bagchi ◽  
Quentin Corbel ◽  
Imroze Khan ◽  
Ellen Payne ◽  
Devshuvam Banerji ◽  
...  
Keyword(s):  
Sex Differences ◽  
Sexual Dimorphism ◽  
Mating System ◽  
Sexual Conflict ◽  
Experimental Evolution ◽  
Parasitic Infections ◽  
Pathogen Dynamics ◽  
Trade Offs ◽  
Host Pathogen ◽  
Seed Beetles

Abstract Background Sexual dimorphism in immunity is believed to reflect sex differences in reproductive strategies and trade-offs between competing life history demands. Sexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex differences in immunity as well as associated host–pathogen dynamics. Yet, experimental evidence linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females. Results We demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males. This difference is accompanied by concomitant sex differences in the expression of genes in the prophenoloxidase activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (resulting in low remating rates and reduced sexual conflict relative to natural polygamy) rapidly decreases female (but not male) PO activity. Moreover, monogamous females had evolved increased tolerance to bacterial infection unrelated to mating, implying that female responses to costly mating may trade off with other aspects of immune defence, an hypothesis which broadly accords with the documented sex differences in gene expression. Finally, female (but not male) PO activity shows correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects. Conclusions Our study provides insights into the links between sexual conflict and sexual dimorphism in immunity and suggests that selection pressures moulded by mating interactions can lead to a sex-specific mosaic of immune responses with important implications for host–pathogen dynamics in sexually reproducing organisms.

scholarly journals Evolutionary change in the construction of the nursery environment when parents are prevented from caring for their young directly

2021 ◽  
Vol 118 (48) ◽  
pp. e2102450118
Author(s):  
Ana Duarte ◽  
Darren Rebar ◽  
Allysa C. Hallett ◽  
Benjamin J. M. Jarrett ◽  
Rebecca M. Kilner
Keyword(s):  
Parental Care ◽  
Experimental Evolution ◽  
Evolutionary Change ◽  
Direct Care ◽  
Dead Body ◽  
Extended Phenotype ◽  
Burying Beetle ◽  
Burying Beetles ◽  
Nicrophorus Vespilloides ◽  
Cross Fostering

Parental care can be partitioned into traits that involve direct engagement with offspring and traits that are expressed as an extended phenotype and influence the developmental environment, such as constructing a nursery. Here, we use experimental evolution to test whether parents can evolve modifications in nursery construction when they are experimentally prevented from supplying care directly to offspring. We exposed replicate experimental populations of burying beetles (Nicrophorus vespilloides) to different regimes of posthatching care by allowing larvae to develop in the presence (Full Care) or absence of parents (No Care). After only 13 generations of experimental evolution, we found an adaptive evolutionary increase in the pace at which parents in the No Care populations converted a dead body into a carrion nest for larvae. Cross-fostering experiments further revealed that No Care larvae performed better on a carrion nest prepared by No Care parents than did Full Care larvae. We conclude that parents construct the nursery environment in relation to their effectiveness at supplying care directly, after offspring are born. When direct care is prevented entirely, they evolve to make compensatory adjustments to the nursery in which their young will develop. The rapid evolutionary change observed in our experiments suggests there is considerable standing genetic variation for parental care traits in natural burying beetle populations—for reasons that remain unclear.

scholarly journals Adaptation to temporally fluctuating environments by the evolution of maternal effects

2015 ◽  
Author(s):  
Snigdhadip Dey ◽  
Steve Proulx ◽  
Henrique Teotonio
Keyword(s):  
Maternal Effects ◽  
Experimental Evolution ◽  
Reproductive Strategies ◽  
Correlated Response ◽  
Bet Hedging ◽  
Offspring Performance ◽  
Trade Offs ◽  
Wide Range ◽  
Fluctuating Environments ◽  
Selection For

Most organisms live in ever-challenging temporally fluctuating environments. Theory suggests that the evolution of anticipatory (or deterministic) maternal effects underlies adaptation to environments that regularly fluctuate every other generation because of selection for increased offspring performance. Evolution of maternal bet-hedging reproductive strategies that randomize offspring phenotypes is in turn expected to underlie adaptation to irregularly fluctuating environments. Although maternal effects are ubiquitous their adaptive significance is unknown since they can easily evolve as a correlated response to selection for increased maternal performance. Using the nematode Caenorhabditis elegans, we show the experimental evolution of maternal provisioning of offspring with glycogen, in populations facing a novel anoxia hatching environment every other generation. As expected with the evolution of deterministic maternal effects, improved embryo hatching survival under anoxia evolved at the expense of fecundity and glycogen provisioning when mothers experienced anoxia early in life. Unexpectedly, populations facing an irregularly fluctuating anoxia hatching environment failed to evolve maternal bet-hedging reproductive strategies. Instead, adaptation in these populations should have occurred through the evolution of balancing trade-offs over multiple generations, since they evolved reduced fitness over successive generations in anoxia but did not go extinct during experimental evolution. Mathematical modelling confirms our conclusion that adaptation to a wide range of patterns of environmental fluctuations hinges on the existence of deterministic maternal effects, and that they are generally much more likely to contribute to adaptation than maternal bet-hedging reproductive strategies.

scholarly journals Host heterogeneity mitigates virulence evolution

2020 ◽  
Vol 16 (1) ◽  
pp. 20190744 ◽  
Author(s):  
P. Signe White ◽  
Angela Choi ◽  
Rishika Pandey ◽  
Arthur Menezes ◽  
McKenna Penley ◽  
...  
Keyword(s):  
Experimental Evolution ◽  
Parasite Prevalence ◽  
Mixed Genotype ◽  
Selective Pressures ◽  
Virulence Evolution ◽  
Specific Host ◽  
Trade Offs ◽  
Evolutionary Trajectories ◽  
Parasite Populations ◽  
Host Heterogeneity

Parasites often infect genetically diverse host populations, and the evolutionary trajectories of parasite populations may be shaped by levels of host heterogeneity. Mixed genotype host populations, compared to homogeneous host populations, can reduce parasite prevalence and potentially reduce rates of parasite adaptation due to trade-offs associated with adapting to specific host genotypes. Here, we used experimental evolution to select for increased virulence in populations of the bacterial parasite Serratia marcescens exposed to either heterogeneous or homogeneous populations of Caenorhabditis elegans . We found that parasites exposed to heterogeneous host populations evolved significantly less virulence than parasites exposed to homogeneous host populations over several hundred bacterial generations. Thus, host heterogeneity impeded parasite adaptation to host populations. While we detected trade-offs in virulence evolution, parasite adaptation to two specific host genotypes also resulted in modestly increased virulence against the reciprocal host genotypes. These results suggest that parasite adaptation to heterogeneous host populations may be impeded by both trade-offs and a reduction in the efficacy of selection as different host genotypes exert different selective pressures on a parasite population.

Host manipulation by Ligula intestinalis: accident or adaptation?

Parasitology ◽  
2001 ◽  
Vol 123 (5) ◽  
pp. 519-529 ◽  
Author(s):  
S. P. BROWN ◽  
G. LOOT ◽  
B. T. GRENFELL ◽  
J. F. GUÉGAN
Keyword(s):  
Linear Models ◽  
Rutilus Rutilus ◽  
Infected Fish ◽  
Life Cycles ◽  
Fish Host ◽  
Host Manipulation ◽  
Ligula Intestinalis ◽  
Game Theoretic ◽  
Effect Hypothesis ◽  
The Impact

Numerous studies have demonstrated that parasites with complex life-cycles can cause phenotypic modifications in their hosts that lead to an increased rate of transmission, and suggest that these modifications are the result of parasitic adaptations to manipulate the host. Little attention is paid, however, to separating the possibility of adaptive host manipulation from incidental (if fortuitous) side-effects of infection. In this study we combine statistical and analytical tools to interpret the impact of the macroparasite Ligula intestinalis L. (Cestoda, Pseudophyllidea) on the behaviour of its intermediate fish host (the roach, Rutilus rutilus L.), using field data on a natural system. Two distinct sets of generalized linear models agree that both the presence and the intensity of infection contribute to a modified behavioural response in the host. This was illustrated by a preference for the lake-edge in infected fish during autumn. Furthermore, the effect of parasites upon their host is heterogeneous with respect to parasite size, with larger parasite individuals having a disproportionate impact. A series of game-theoretic models of adaptive host manipulation illustrate a potential rationale for a size-dependent manipulation strategy in parasites. These findings illustrate the potential complexity and functionality of the impact of L. intestinalis upon its fish host, which together reduce the parsimony of the alternative ‘incidental effect’ hypothesis.

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