Immune activation decreases sperm viability in both sexes and influences female sperm storage

Radhakrishnan, Preethi; Fedorka, Kenneth M.

doi:10.1098/rspb.2012.0654

Cited by 37 publications

(46 citation statements)

References 42 publications

(43 reference statements)

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“…being immunocompromised). If immune activation disrupts reproductive tissues and output [30, 31], such processes would be strongly selected against due to their fitness consequences. Under this hypothesis, JH may act to suppress immune signaling to prevent instances of autoimmunity, especially in cases where reproductive tissues may be targeted.…”

Section: Resultsmentioning

confidence: 99%

Juvenile Hormone Suppresses Resistance to Infection in Mated Female Drosophila melanogaster

2017

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Summary Hormonal signaling provides metazoans with the ability to regulate development, growth, metabolism, immune defense, and reproduction in response to internal and external stimuli. The use of hormones as central regulators of physiology makes them prime candidates for mediating allocation of resources to competing biological functions (i.e. hormonal pleiotropy) [1]. In animals, reproductive effort often results in weaker immune responses (e.g. [2–4]) and this reduction is sometimes linked to hormone signaling (see [5–7]). In the fruit fly, Drosophila melanogaster, mating and the receipt of male seminal fluid proteins results in reduced resistance to a systemic bacterial infection [8, 9]. Here, we evaluate whether the immunosuppressive effect of reproduction in female D. melanogaster is attributable to the endocrine signal juvenile hormone (JH), which promotes the development of oocytes and the synthesis and deposition of yolk protein [10, 11]. Previous work has implicated JH as immunosuppressive [12, 13], and the male seminal fluid protein Sex Peptide (SP) activates JH biosynthesis in female D. melanogaster after mating [14]. We find that transfer of SP activates synthesis of JH in the mated female, which in turn suppresses resistance to infection through the receptor germ cell-expressed (gce). We find that mated females are more likely to die from infection, suffer higher pathogen burdens, and are less able to induce their immune responses. All of these deficiencies are rescued when JH signaling is blocked. We argue that hormonal signaling is important for regulating immune system activity and, more generally, for governing trade-offs between physiological processes.

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Section: Resultsmentioning

confidence: 99%

Juvenile Hormone Suppresses Resistance to Infection in Mated Female Drosophila melanogaster

2017

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“…To this end, flies were lightly CO 2 anesthetized and a 0.2 mm diameter needle (Fine Science Tools) was dipped in bacterial solution and inserted into the mesopleuron below the wing [methods similar to those of Radhakrishnan and Fedorka (Radhakrishnan and Fedorka, 2012)]. To create the LD 50 concentration, bacteria were incubated in sterilized LB broth at 37°C until log phase.…”

Section: Immune Assaymentioning

confidence: 99%

Thermoregulatory strategy may shape immune investment inDrosophila melanogaster

Kutch

Sevgili

Wittman

et al. 2014

Journal of Experimental Biology

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As temperatures change, insects alter the amount of melanin in their cuticle to improve thermoregulation. However, melanin is also central to insect immunity, suggesting that thermoregulatory strategy may indirectly impact immune defense by altering the abundance of melanin pathway components (a hypothesis we refer to as thermoregulatory-dependent immune investment). This may be the case in the cricket Allonemobius socius, where warm environments (both seasonal and geographical) produced crickets with lighter cuticles and increased pathogen susceptibility. Unfortunately, the potential for thermoregulatory strategy to influence insect immunity has not been widely explored. Here we address the relationships between temperature, thermoregulatory strategy and immunity in the fruit fly Drosophila melanogaster. To this end, flies from two separate Canadian populations were reared in either a summer-or autumnlike environment. Shortly after adult eclosion, flies were moved to a common environment where their cuticle color and susceptibility to a bacterial pathogen (Pseudomonas aeruginosa) were measured. As with A. socius, individuals from summer-like environments exhibited lighter cuticles and increased pathogen susceptibility, suggesting that the thermoregulatory-immunity relationship is evolutionarily conserved across the hemimetabolous and holometabolous clades. If global temperatures continue to rise as expected, then thermoregulation might play an important role in host infection and mortality rates in systems that provide critical ecosystem services (e.g. pollination), or influence the prevalence of insect-vectored disease (e.g. malaria).

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“…Notwithstanding this, we acknowledge that other studies have previously tested for plasticity in traits tied to male reproductive success, following exposure to nonpathogenic immune elicitors. Many of these have focused on components of sperm quality, and they have generally recorded negative effects of a pathogen exposure; for example, in studies of fruit flies, D. melanogaster (Radhakrishnan & Fedorka, ), moths, Heliothis armigera (McNamara, van Lieshout, Jones, & Simmons, ), house crickets, Gryllodes sigillatus (Kerr, Gershman, & Sakaluk, ), and field crickets, Telegryllus oceanicus (Simmons, ). Other studies have explored the effects of noninfectious challenges on male mate calling patterns in crickets, and these have also observed effects linked to exposure.…”

Section: Discussionmentioning

confidence: 99%

The effects of a bacterial challenge on reproductive success of fruit flies evolved under low or high sexual selection

Nystrand

Cassidy

Dowling

2018

Ecology and Evolution

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The capacity of individuals to cope with stress, for example, from pathogen exposure, might decrease with increasing levels of sexual selection, although it remains unclear which sex should be more sensitive. Here, we measured the ability of each sex to maintain high reproductive success following challenges with either heat‐killed bacteria or procedural control, across replicate populations of Drosophila melanogaster evolved under either high or low levels of sexual selection. Our experiment was run across four separate sampling blocks. We found an interaction between bacterial treatment, sexual selection treatment, and sampling block on female reproductive success. Specifically, and only in the fourth block, we observed that bacterial‐challenged females that had evolved under high sexual selection, exhibited lower reproductive success than bacterial‐challenged females that had evolved under low sexual selection. Furthermore, we could trace this block‐specific effect to a reduction in viscosity of the ovipositioning substrate in the fourth block, in which females laid around 50% more eggs than in previous blocks. In contrast, patterns of male reproductive success were consistent across blocks. Males that evolved under high sexual selection exhibited higher reproductive success than their low‐selection counterparts, regardless of whether they were subjected to a bacterial challenge or not. Our results are consistent with the prediction that heightened sexual selection will invoke male‐specific evolutionary increases in reproductive fitness. Furthermore, our findings suggest that females might pay fitness costs when exposed to high levels of sexual selection, but that these costs may lie cryptic, and only be revealed under certain environmental contexts.

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Immune activation decreases sperm viability in both sexes and influences female sperm storage

Cited by 37 publications

References 42 publications

Juvenile Hormone Suppresses Resistance to Infection in Mated Female Drosophila melanogaster

Juvenile Hormone Suppresses Resistance to Infection in Mated Female Drosophila melanogaster

Thermoregulatory strategy may shape immune investment inDrosophila melanogaster

The effects of a bacterial challenge on reproductive success of fruit flies evolved under low or high sexual selection

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