A possible tradeoff between developmental rate and pathogen resistance in Drosophila melanogaster

Modak, Shampa Ghosh; Satish, Kumar; Mohan, J.; Dey, Sutirth; Raghavendra, N.; Shakarad, Mallikarjun; Joshi, Amitabh

doi:10.1007/s12041-009-0036-8

Cited by 12 publications

(12 citation statements)

References 14 publications

(20 reference statements)

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“…Kraaijeveld et al (2001) hypothesized that the common embryonic origin of the head muscles (used in feeding) and the hemopoietic organ (that produces the hemocytes that are responsible for the cellular immune response) may provide a proximate explanation for any developmental trade-offs in Drosophila. Thus, the relatively smaller size of males in the presence of pathogens is consistent with previous work that has found that flies experimentally evolved in an immunologically challenging environment also exhibited lower feeding rates (Fellowes et al 1999), and that there are developmental trade-offs between growth and immunocompetence (Modak et al 2009). The fact that this phenomenon was only observed in male offspring may reflect the effects of sex-specific selective pressures.…”

Section: Discussionsupporting

confidence: 90%

“…However, both male and female flies in the experimental populations were less resistant to immunological challenge from Escherichia coli than those from the control populations. More recently, Modak et al (2009) compared the resistance to E. coli in flies from populations that had been selected for faster development with those from corresponding control populations. They found that flies from the fast-selected lines exhibited higher rates of pathogen-induced mortality than did those from controls, suggestive of a genetic correlation between development rate and pathogen resistance.…”

Section: Introductionmentioning

confidence: 99%

“…Overall, these various experiments suggest that the components of life history (mating success, body size, immunocompetence, and development rate) are linked. However, the magnitude and sign of these relationships remain unclear, as together these studies indicate that selection for increased male attractiveness may cause decreased immunocompetence (McKean and Nunney 2008), selection for increased immunocompetence may lead to increased male attractiveness (Rolff and Kraaijeveld 2003), and that decreased immunocompetence is correlated with a increased development rate and smaller body size (Modak et al 2009). …”

Section: Introductionmentioning

confidence: 99%

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Cross-generational effects of male reproductive success and offspring immunocompetence inDrosophila melanogaster

Guncay

Balasubramaniam

Plagens

et al. 2017

FACETS

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In some species where males make no direct contribution to a female's lifetime reproductive success, females choose mates based on the indirect benefits manifested in their offspring. One trait that may be subject to this sexual selection is immunocompetence (the ability to mount an immune response following exposure to pathogens); however, the results of previous work on its link to male attractiveness have been ambiguous. Herein we examine the life history consequences of mating with males with a history of failure or success in reproductive competitions in Drosophila melanogaster. By examining egg-to-adult survival, body weights, and bacterial loads of offspring reared in either the absence or presence of a bacterial pathogen, we were able to examine whether sire reproductive success was associated with their offsprings' ability to respond to an immunological challenge and other life history traits. Our results are partially consistent with the predictions of the "immunocompetence handicap hypothesis": competitively successful males ("studs") sire male offspring that are better able to handle an immunological challenge than those sired by competitively unsuccessful males ("duds"). However, our assay also revealed the opposite pattern in female offspring, suggestive of the complicating presence of alleles with sexually antagonistic effects on the expression of this important life history trait.

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Section: Discussionsupporting

confidence: 90%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Cross-generational effects of male reproductive success and offspring immunocompetence inDrosophila melanogaster

Guncay

Balasubramaniam

Plagens

et al. 2017

FACETS

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“…Populations of D. melanogaster have been used for artificial selection for resistance to infection by microbes or parasitoids, and the evolution of other fitness-related traits is a typical result of such studies (summarized by McKean and Lazzaro [16]). Conversely, artificial selection on life history traits can affect immunity; Modak et al [17] documented that D. melanogaster selected for decreased development time exhibited a shorter time to death following introduction of E. coli than unselected controls. In the present study, lines of D. melanogaster selected for survival after introduction of B. cereus tended to have decreased incidence of progeny that acquired DMelSV.…”

Section: Discussionmentioning

confidence: 99%

Sigma Virus (DMelSV) Incidence in Lines of Drosophila melanogaster Selected for Survival following Infection with Bacillus cereus

Bentz

Humphrey

Harshman

et al. 2017

Psyche: A Journal of Entomology

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The immune response of Drosophila melanogaster is complex and involves both specific and general responses to parasites. In this study we tested for cross-immunity for bacteria and viruses by scoring the incidence of infection with the vertically transmitted Sigma virus (DMelSV) in the progeny of a cross between females transmitting DMelSV at high frequencies and males from lines subjected to three selection regimes related to resistance to Bacillus cereus. There was no significant difference in transmission of DMelSV among selection regimes, though results suggest that the B. cereus selected lines had lower rates of infection by DMelSV. We found a significant difference in viral infection with respect to the sex of the progeny, with males consistently less likely to be infected than females. Given a finite energy budget, flies that have experienced immune system challenge may show alterations in other life history traits. Later eclosing progeny were also less likely to be infected than earlier eclosing progeny, indicating a relationship with development time. Finally, there was a significant interaction between the timing of collection and the sex of the progeny, such that later eclosing males were the most resistant group. Increased development time is sometimes associated with increased energy acquisition; from this perspective, increased development time may be associated with acquiring sufficient resources for effective resistance.

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“…This notion underlies the theory of optimal immune defense (e.g., Viney et al 2005;Donnelly et al 2017), as well as some of the theories linking heritable pathogen resistance with sexually selected traits (Folstad and Karter 1992;Westneat and Birkhead 1998;Adamo and Spiteri 2005). It is supported by extensive evidence from genetic analyses and selection experiments that found negative genetic correlations between pathogen resistance and survival, growth, developmental rate, fecundity or longevity, often amplified under nutritional or other stress (Kraaijeveld and Godfray 2008;Vorburger et al 2008;Modak et al 2009;Ye et al 2009;Hall et al 2010;Boots 2011;Duncan et al 2011;Auld et al 2013;Vijendravarma et al 2015;McGonigle et al 2017;McNamara and Simmons 2017;Bartlett et al 2018; older studies reviewed in Lazzaro and Little 2009).…”

mentioning

confidence: 87%

Sexual selection reveals a cost of pathogen resistance undetected in life‐history assays

Kawecki

2019

Evolution

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Mechanisms of resistance to pathogens and parasites are thought to be costly and thus to lead to evolutionary trade‐offs between resistance and life‐history traits expressed in the absence of the infective agents. On the other hand, sexually selected traits are often proposed to indicate “good genes” for resistance, which implies a positive genetic correlation between resistance and success in sexual selection. Here I show that experimental evolution of improved resistance to the intestinal pathogen Pseudomonas entomophila in Drosophila melanogaster was associated with a reduction in male sexual success. Males from four resistant populations achieved lower paternity than males from four susceptible control populations in competition with males from a competitor strain, indicating an evolutionary cost of resistance in terms of mating success and/or sperm competition. In contrast, no costs were found in larval viability, larval competitive ability and population productivity assayed under nutritional limitation; together with earlier studies this suggests that the costs of P. entomophila resistance for nonsexual fitness components are negligible. Thus, rather than indicating heritable pathogen resistance, sexually selected traits expressed in the absence of pathogens may be sensitive to costs of resistance, even if no such costs are detected in other fitness traits.

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A possible tradeoff between developmental rate and pathogen resistance in Drosophila melanogaster

Cited by 12 publications

References 14 publications

Cross-generational effects of male reproductive success and offspring immunocompetence inDrosophila melanogaster

Cross-generational effects of male reproductive success and offspring immunocompetence inDrosophila melanogaster

Sigma Virus (DMelSV) Incidence in Lines of Drosophila melanogaster Selected for Survival following Infection with Bacillus cereus

Sexual selection reveals a cost of pathogen resistance undetected in life‐history assays

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