Cold‐seeking behaviour mitigates reproductive losses from fungal infection in Drosophila

Abstract

Summary Animals must tailor their life‐history strategies to suit the prevailing conditions and respond to hazards in the environment. Animals with lethal infections are faced with a difficult choice: to allocate more resources to reproduction and suffer higher mortality or to reduce reproduction with the expectation of enhanced immunity and late‐age reproduction. However, the strategies employed to mediate shifts in life‐history traits are largely unknown.Here, we investigate the temperature preference of the fruit fly, Drosophila melanogaster, during infection with the fungal pathogen, Metarhizium robertsii, and the consequence of temperature preference on life‐history traits.We have measured the temperature preference of fruit flies under different pathogen conditions. We conducted multiple fitness assays of the host and the pathogen under different thermal conditions. From these data, we estimated standard measures of fitness and used age‐specific methodologies to test for the fitness trade‐offs that are thought to underlie differences in life‐history strategy.We found that fungus‐infected fruit flies seek out cooler temperatures, which facilitates an adaptive shift in their life‐history strategy. The colder temperatures preferred by infected animals were detrimental to the pathogen because it increased resistance to infection. But, it did not provide net benefits that were specific to infected animals, as cooler temperatures increased lifetime reproductive success and survival whether or not the animals were infected. Instead, we find that cold‐seeking benefits infected animals by increasing their late‐age reproductive output, at a cost to their early‐age reproductive output. In contrast, naive control flies prefer warmer temperatures that optimize early‐age reproductive, at a cost to reproductive output at late ages.These findings show that infected animals exhibit fundamentally different reproductive strategies than their healthy counterparts. Temperature preference can facilitate shifts in strategy, but not without inevitable trade‐offs.

Fungal infection dynamics in response to temperature in the lepidopteran insect Galleria mellonella

“…These changes in thermal regime usually favor the immune response and promote host survival, but not all insects exhibit behavioral thermoregulation, and where it is reported it is often at a cost to the host (Blandford et al ., ; Anderson et al ., , b). Some insects seek lower temperature environments that presumably slow down fungal development, giving the insect more time to mount an effective defense response to resist the pathogen (Hunt et al ., ). Quite a few insects do not regulate temperature but their survival is vastly improved if kept at higher temperatures, as reported for the Asian longhorned beetle, Anoplophora glabripennis (Motschulsky) exposed to Metarhizium brunneum (Fisher & Hajek, ).…”

Interplay between Fungal Infection and Bacterial Associates in the Wax Moth Galleria mellonella under Different Temperature Conditions

“…Temperature is one of the crucial factors that influences the development of mycoses and bacterioses in insects. Temperature acts on both microorganism growth and on insect immune and behavioral reactions [ 9 , 10 , 11 , 12 , 13 , 14 ]. Entomopathogenic ascomycetes usually have optimal growth between 20–30 °C [ 15 ].…”

Characterisation and evaluation of Metarhizium anisopliae (Metsch.) Sorokin strains for their temperature tolerance

“…Behavioural adaptations of some insect hosts (like locusts) increasing their body temperature to counter fungal pathogens underlines the importance of temperature (Rangel et al 2010). In contrast, infected drosophila flies displayed behaviour of moving to cooler places to enhance immunity (Hunt et al 2016). The ability of the certain strains of EPF to grow and sporulate under a wide temperature ranges is very useful in their application as biological control agents particularly in semi-arid climates.…”