The transgenerational consequences of maternal parasitism for aphid life history and suitability for subsequent parasitism

Aphids parasitized in later instars can give birth to several nymphs before their reproduction is curtailed by the developing parasitoid. We examined the life histories of Aphis fabae Scopoli born to mothers parasitized by Lysiphlebus fabarum Marshall, and their suitability as subsequent hosts, to test the ‘fecundity compensation’ hypothesis. Maternal parasitism negatively impacted life history parameters, resulting in reduced estimates of population increase (rm, R0, and λ), and increased generation time (GT) and doubling time (DT). These impacts were greater when the larva developing in the mother turned out to be female rather than male, and greater still when mothers were superparasitized. Maternal parasitism produced aphids with shorter hind tibia (HTL), at birth and at maturity, but their developmental time was unaffected. Although female L. fabarum readily accepted such aphids for oviposition, rates of mummification and wasp emergence were lower, and more so when the maternal parasitoid was female. The resulting parasitoids took longer to develop than progeny from control wasps, had shorter HTLs, lower egg loads, smaller eggs, and produced fewer mummies with lower rates of adult emergence, all differences that were more pronounced when the maternal parasitoid was female. The progeny of these wasps exhibited similar impairments to these biological parameters as their parents, demonstrating that the negative impacts of development in maternally parasitized hosts extended for at least two generations. Thus, our results do not support fecundity compensation, but suggest that any benefits of post-parasitism reproduction will be offset by reduced fitness in both aphid progeny and the parasitoids that develop in them.

Fight or Flight? Alternative Defense of the Pea Aphids, Acyrthosiphon pisum on Different Host Plants

Non-immunological responses are important alternative strategies for animals to deal with pathogens. It has long been recognized that fecundity compensation and production of winged offspring are two common non-immunological responses used by aphids when confronted with predators or pathogens. However, the effects of host plant on these responses have received little attention. This study investigated the effects of host plant on non-immunological defense in the pea aphids, Acyrthosiphon pisum, after bacterial and fungal infections. The aphids were raised in two groups, with one group being raised on broad beans and the other group being raised on alfalfa. The secondary symbiont background was examined, and the aphids were then infected with bacteria and fungus to assess fecundity and winged offspring production. We found that aphids that had been fed alfalfa had fewer offspring than those fed broad beans. Alfalfa-fed aphids produced more winged offspring in response to S. aureus and B. bassiana infections. Our findings suggest that the host plant plays a key role in fecundity and winged offspring production in pea aphid colony.

Lack of Host Reproductive Trade-offs Associated with Fecundity Compensation Response to Parasitic Castration

Host-parasite coevolution may result in life-history changes in hosts that can limit the detrimental effects of parasitism. Fecundity compensation is one such life-history response, occurring when hosts increase their current reproductive output to make up for expected losses in future reproduction due to parasitic infection. However, the potential trade-offs between quantity and quality of offspring produced during fecundity compensation are relatively unexplored. This study uses the trematode, Schistosoma mansoni, and its snail intermediate host, Biomphalaria glabrata, to better understand the impacts of this host life-history response. Measures of host reproductive output as well as offspring hatching success and survival were collected to assess the reproductive consequences of infection. Infected snails exhibited fecundity compensation (increase in the number of eggs laid compared to controls) and had a higher probability of laying any eggs at all. Infection status did not play a significant role in hatching or offspring survival to maturity. However, the age of the parental snail had a significant impact on hatching success, as offspring from older parents demonstrated a higher hatching success rate. Overall, the lack of an apparent trade-off between quantity and quality of offspring suggests that infected parental snails invest more resources towards reproduction in order to maintain the fitness of their offspring, possibly at the expense of their own longevity.

Lack of trade-offs in host offspring produced during fecundity compensation

Host–parasite coevolution may result in life-history changes in hosts that can limit the detrimental effects of parasitism. Fecundity compensation is one such life-history response, occurring when hosts increase their current reproductive output to make up for expected losses in future reproduction due to parasitic infection. However, the potential trade-offs between this increase in quantity and the quality of offspring have been relatively unexplored. This study uses the trematode, Schistosoma mansoni, and its snail intermediate host, Biomphalaria glabrata, to better understand how this host life-history response, fecundity compensation, impacts host reproduction. Measures of host reproductive output as well as offspring hatching success and survival were collected to assess the reproductive consequences of infection. Infected snails exhibited fecundity compensation by increasing the number of eggs laid and the overall probability of laying eggs compared to uninfected snails. Parental infection status did not play a significant role in hatching or offspring survival to maturity. Offspring from a later reproductive bout demonstrated a higher hatching success rate. Overall, the lack of an apparent trade-off between quantity and quality of offspring suggests that infected parental snails invest more resources towards reproduction not only to increase reproductive output, but also to maintain the fitness of their offspring, possibly at the expense of their own longevity.

Snail host parental investment throughout a Schistosoma mansoni infection

Parental investment theory describes the ability of organisms to respond to an environmental challenge by increasing the fitness of future offspring. Utilizing life history changes, organisms can maximize fitness by increasing their total reproductive output or by investing more into the success of fewer offspring. In cases where parasitic infections result in castration of their host, increased reproductive effort known as fecundity compensation has been demonstrated in a variety of organisms. This response appears predictive of expected future reproductive losses. Organisms struggling with an environmental pathogen, may attempt to better prepare their offspring for the environment they are experiencing through transgenerational immune priming (TGIP). In immune priming, primary infection lowers the prevalence and intensity of a subsequent infection by the same pathogen. Transgenerational immune priming carries pathogen resistance into further generations without genotypic changes. The focus of this study was to determine whether invertebrate parental investment into offspring parasite resistance varies over the course of an infection. Utilizing the snail host Biomphalaria glabrata and its trematode parasite Schistosoma mansoni, offspring were reared from specific time intervals in the parent’s infection and subsequently exposed to the same pathogen when each cohort reached the same age- 12 weeks. Differences in infection prevalence and intensity were expected based on when the offspring were born during their parent’s infection. A trade-off was predicted between the number of offspring produced in a cohort and offspring resistance to future infections. Offspring born during the period of fecundity compensation were predicted to exhibit lower resistance due to a dilution of individual investment by parents into a larger offspring pool. While our results did not support TGIP, there were differences in offspring prevalence, as well as an indication that parent health may interact with genetics in offspring resistance. Results suggest that parental condition can influence resistance of B. glabrata offspring to S. mansoni but that TGIP may not be operating in this system.

Stomach nematodes of cotton rats: parasites, commensals, or mutualists?

We related presence and burden of stomach nematodes to body mass and reproductive allocation in hispid cotton rats (Sigmodon hispidus) from two long-running field studies in Virginia (1983–1984, n = 286; and 1988–1990, n = 425) and one from Georgia 1987–1989 (n = 459). Eighty percent of rats from the earlier Virginia sample were infected, with mean nematode mass of 1,311 mg. In the later samples, 23% (Virginia) and 33% (Georgia) were infected with mean nematode mass of 493 and 769 mg, respectively. Presence of nematodes was positively correlated with host body length for each sex in each sample. We used analysis of covariance to examine length-adjusted residuals for presence of nematodes and mass of nematodes for association with somatic and reproductive response variables. Both body and reproductive masses were either positively associated or not related to nematode presence in the two low-prevalence samples, and either negatively associated or not related to nematode presence in the high-prevalence sample. No relationships were detected between host mass and nematode mass per host in either sex in any sample. There was no effect of nematode presence on litter size of pregnant females, but there was a positive effect of nematode mass on litter size in Georgia. Recent theory provides several possible explanations for such neutral-to-positive effects of stomach nematodes on host fitness, including the evolution of host tolerance to the parasites, fecundity compensation by the hosts, and positive effects on host health via immune modulation.

A highly infective plant-associated bacterium influences reproductive rates in pea aphids

Pea aphids, Acyrthosiphon pisum , have the potential to increase reproduction as a defence against pathogens, though how frequently this occurs or how infection with live pathogens influences this response is not well understood. Here we determine the minimum infective dose of an environmentally common bacterium and possible aphid pathogen, Pseudomonas syringae , to determine the likelihood of pathogenic effects to pea aphids. Additionally, we used P. syringae infection to investigate how live pathogens may alter reproductive rates. We found that oral bacterial exposure decreased subsequent survival of aphids in a dose-dependent manner and we estimate that ingestion of less than 10 bacterial cells is sufficient to increase aphid mortality. Pathogen dose was positively related to aphid reproduction. Aphids exposed to low bacterial doses showed decreased, although statistically indistinguishable, fecundity compared to controls. Aphids exposed to high doses reproduced significantly more than low dose treatments and also more, but not significantly so, than controls. These results are consistent with previous studies suggesting that pea aphids may use fecundity compensation as a response to pathogens. Consequently, even low levels of exposure to a common plant-associated bacterium may therefore have significant effects on pea aphid survival and reproduction.