Limits...
Disease and the extended phenotype: parasites control host performance and survival through induced changes in body plan.

Goodman BA, Johnson PT - PLoS ONE (2011)

Bottom Line: Malformed frogs exhibited significantly shorter jumping distances (41% reduction), slower swimming speeds (37% reduction), reduced endurance (66% reduction), and lower foraging success relative to infected hosts without malformations.Our results highlight the ability of parasites to deeply alter multiple dimensions of host phenotype with important consequences for performance and survival.These patterns were best explained by malformation status, rather than infection per se, helping to decouple the direct and indirect effects of parasitism on host fitness.

View Article: PubMed Central - PubMed

Affiliation: Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, United States of America.

ABSTRACT

Background: By definition, parasites harm their hosts. However, some forms of parasite-induced alterations increase parasite transmission between hosts, such that manipulated hosts can be considered extensions of the parasite's phenotype. While well accepted in principle, surprisingly few studies have quantified how parasite manipulations alter host performance and survival under field and laboratory conditions.

Methodology/principal findings: By interfering with limb development, the trematode Ribeiroia ondatrae causes particularly severe morphological alterations within amphibian hosts that provide an ideal system to evaluate parasite-induced changes in phenotype. Here, we coupled laboratory performance trials with a capture-mark-recapture study of 1388 Pacific chorus frogs (Pseudacris regilla) to quantify the effects of parasite-induced malformations on host locomotion, foraging, and survival. Malformations, which affected ∼ 50% of metamorphosing frogs in nature, caused dramatic reductions in all measures of organismal function. Malformed frogs exhibited significantly shorter jumping distances (41% reduction), slower swimming speeds (37% reduction), reduced endurance (66% reduction), and lower foraging success relative to infected hosts without malformations. Furthermore, while normal and malformed individuals had comparable survival within predator-free exclosures, deformed frogs in natural populations had 22% lower biweekly survival than normal frogs and rarely recruited to the adult population over a two-year period.

Conclusions/significance: Our results highlight the ability of parasites to deeply alter multiple dimensions of host phenotype with important consequences for performance and survival. These patterns were best explained by malformation status, rather than infection per se, helping to decouple the direct and indirect effects of parasitism on host fitness.

Show MeSH

Related in: MedlinePlus

Effects of limbs malformations on the locomotory performance of Pacific chorus frogs (P. regilla) in laboratory trials.Above: chorus frog with parasite-induced limb malformation. Below: presented are the results of trials measuring (A) maximum burst swim speed, (B) maximum swimming distance, (C) maximum endurance time, and (D) maximum jump distance.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3102088&req=5

pone-0020193-g001: Effects of limbs malformations on the locomotory performance of Pacific chorus frogs (P. regilla) in laboratory trials.Above: chorus frog with parasite-induced limb malformation. Below: presented are the results of trials measuring (A) maximum burst swim speed, (B) maximum swimming distance, (C) maximum endurance time, and (D) maximum jump distance.

Mentions: Of the 114 frogs used in performance trials, 63 were normal and 51 exhibited one or more malformations. Malformations affected the hind limbs and were dominated by extra limbs or feet (52.1%) and skin webbings (21.1%) (n = 71 total abnormalities) (Fig. 1). We found no differences in the initial mass or length of malformed and normal frogs (Mass: F 1, 114 = 1.183, P = 0.279; SUL: F 1, 114 = 0.637, P = 0.427). Among the subsample of frogs collected prior to initiating performance trials, we also found no difference in R. ondatrae metacercarial abundance between normal and malformed frogs (Mean infection in normal and malformed frogs = 36.2 and 42.4, respectively; t = −0.749, P = 0.461). We also found no differences in infection by other larval trematodes, including Alaria sp., Manodistomum sp. and kidney-infecting echinostomes (all P>0.05). No nematodes, cestodes, or adult trematodes were recovered (although we cannot eliminate the possibility of differences in viral, bacterial, or fungal infections).


Disease and the extended phenotype: parasites control host performance and survival through induced changes in body plan.

Goodman BA, Johnson PT - PLoS ONE (2011)

Effects of limbs malformations on the locomotory performance of Pacific chorus frogs (P. regilla) in laboratory trials.Above: chorus frog with parasite-induced limb malformation. Below: presented are the results of trials measuring (A) maximum burst swim speed, (B) maximum swimming distance, (C) maximum endurance time, and (D) maximum jump distance.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3102088&req=5

pone-0020193-g001: Effects of limbs malformations on the locomotory performance of Pacific chorus frogs (P. regilla) in laboratory trials.Above: chorus frog with parasite-induced limb malformation. Below: presented are the results of trials measuring (A) maximum burst swim speed, (B) maximum swimming distance, (C) maximum endurance time, and (D) maximum jump distance.
Mentions: Of the 114 frogs used in performance trials, 63 were normal and 51 exhibited one or more malformations. Malformations affected the hind limbs and were dominated by extra limbs or feet (52.1%) and skin webbings (21.1%) (n = 71 total abnormalities) (Fig. 1). We found no differences in the initial mass or length of malformed and normal frogs (Mass: F 1, 114 = 1.183, P = 0.279; SUL: F 1, 114 = 0.637, P = 0.427). Among the subsample of frogs collected prior to initiating performance trials, we also found no difference in R. ondatrae metacercarial abundance between normal and malformed frogs (Mean infection in normal and malformed frogs = 36.2 and 42.4, respectively; t = −0.749, P = 0.461). We also found no differences in infection by other larval trematodes, including Alaria sp., Manodistomum sp. and kidney-infecting echinostomes (all P>0.05). No nematodes, cestodes, or adult trematodes were recovered (although we cannot eliminate the possibility of differences in viral, bacterial, or fungal infections).

Bottom Line: Malformed frogs exhibited significantly shorter jumping distances (41% reduction), slower swimming speeds (37% reduction), reduced endurance (66% reduction), and lower foraging success relative to infected hosts without malformations.Our results highlight the ability of parasites to deeply alter multiple dimensions of host phenotype with important consequences for performance and survival.These patterns were best explained by malformation status, rather than infection per se, helping to decouple the direct and indirect effects of parasitism on host fitness.

View Article: PubMed Central - PubMed

Affiliation: Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, United States of America.

ABSTRACT

Background: By definition, parasites harm their hosts. However, some forms of parasite-induced alterations increase parasite transmission between hosts, such that manipulated hosts can be considered extensions of the parasite's phenotype. While well accepted in principle, surprisingly few studies have quantified how parasite manipulations alter host performance and survival under field and laboratory conditions.

Methodology/principal findings: By interfering with limb development, the trematode Ribeiroia ondatrae causes particularly severe morphological alterations within amphibian hosts that provide an ideal system to evaluate parasite-induced changes in phenotype. Here, we coupled laboratory performance trials with a capture-mark-recapture study of 1388 Pacific chorus frogs (Pseudacris regilla) to quantify the effects of parasite-induced malformations on host locomotion, foraging, and survival. Malformations, which affected ∼ 50% of metamorphosing frogs in nature, caused dramatic reductions in all measures of organismal function. Malformed frogs exhibited significantly shorter jumping distances (41% reduction), slower swimming speeds (37% reduction), reduced endurance (66% reduction), and lower foraging success relative to infected hosts without malformations. Furthermore, while normal and malformed individuals had comparable survival within predator-free exclosures, deformed frogs in natural populations had 22% lower biweekly survival than normal frogs and rarely recruited to the adult population over a two-year period.

Conclusions/significance: Our results highlight the ability of parasites to deeply alter multiple dimensions of host phenotype with important consequences for performance and survival. These patterns were best explained by malformation status, rather than infection per se, helping to decouple the direct and indirect effects of parasitism on host fitness.

Show MeSH
Related in: MedlinePlus