Low Temperature Reveals Genetic Variability Against Male-Killing Spiroplasma in Drosophila melanogaster Natural Populations

Abstract

Spiroplasma endosymbionts are maternally inherited microorganisms which infect many arthropod species. In some Drosophila species, it acts as a reproductive manipulator, spreading in populations by killing the sons of infected mothers. Distinct Drosophila melanogaster populations from Brazil exhibit variable male-killing Spiroplasma prevalences. In this study, we investigated the presence of variability for the male-killing phenotype among Drosophila and/or Spiroplasma strains and verified if it correlates with the endosymbiont prevalence in natural populations. For that, we analyzed the male-killing expression when Spiroplasma strains from different populations were transferred to a standard D. melanogaster line (Canton-S) and when a common Spiroplasma strain was transferred to different wild-caught D. melanogaster lines, both at optimal and challenging temperatures for the bacteria. No variation was observed in the male-killing phenotype induced by different Spiroplasma strains. No phenotypic variability among fly lines was detected at optimal temperature (23 °C), as well. Conversely, significant variation in the male-killing expression was revealed among D. melanogaster lines at 18.5 °C, probably caused by imperfect transmission of the endosymbiont. Distinct lines differed in their average sex ratios as well as in the pattern of male-killing expression as the infected females aged. Greater variation occurred among lines from one locality, although there was no clear correlation between the male-killing intensity and the endosymbiont prevalence in each population. Imperfect transmission or male killing may also occur in the field, thus helping to explain the low or intermediate prevalences reported in nature. We discuss the implications of our results for the dynamics of male-killing Spiroplasma in natural populations.

Population Effects of Calcium Phosphate Nanoparticles in Drosophila melanogaster: The Effects of Phase Composition, Crystallinity, and the Pathway of Formation

“…27 Chronic cold exposure can shift the sex ratio toward a male-biased extreme, 28 whereas spiroplasma endosymbionts, the maternally inherited microorganisms that infect arthropod species including Drosophila and act as reproductive manipulators by killing exclusively sons of infected mothers may be a factor involved in this variation. 29 Genotoxic effects have been observed in Drosophila dosed with inorganic nanoparticles, 30−32 but they are improbable to occur with CPs, especially at the low concentration in media of 0.3 wt % used in this study. Even more elevated calcium levels would have been expected to produce a more systemic, cell signaling effect rather than a genotypic one.…”

“…This temperature effect on the fruit fly gender falls under the domain of thermosensitive sex selection, which is frequently used in zoology of fish and reptiles . Chronic cold exposure can shift the sex ratio toward a male-biased extreme, whereas spiroplasma endosymbionts, the maternally inherited microorganisms that infect arthropod species including Drosophila and act as reproductive manipulators by killing exclusively sons of infected mothers may be a factor involved in this variation . Genotoxic effects have been observed in Drosophila dosed with inorganic nanoparticles, − but they are improbable to occur with CPs, especially at the low concentration in media of 0.3 wt % used in this study.…”

The effects of temperature on prevalence of facultative insect heritable symbionts across spatial and seasonal scales

“…Regarding MK, feminization and thelytoky, at permissive temperatures the expression of these phenotypes is close to 100%. When hosts are exposed to both high or low temperatures, the expression of MK by Spiroplasma is greatly reduced (Malogolowkin, 1959;Montenegro and Klaczko, 2004;Anbutsu et al, 2008;Ventura et al, 2014) and exposure to extremely high temperatures reduces the expression of MK by Wolbachia (Hurst et al, 2000(Hurst et al, , 2001. Most studies show that both high and low temperatures reduce the expression of feminization and thelytoky by Wolbachia (Girin and Boulétreau, 1995;Pintureau et al, 1999;Ning et al, 2019;Zhou et al, 2019).…”

From Nature to the Lab: Establishing Drosophila Resources for Evolutionary Genetics

“…In parallel, the development of recombinant inbred lines that constitute the Drosophila Synthetic Population Resource (DSPR) have provided another important resource for the dissection of the genetic basis of complex traits (King et al, 2012;Burke et al, 2014;Marriage et al, 2014;Cogni et al, 2016). Before this, isofemale lines had been at the core of fecund research programs aiming at describing and comparing genomic variation between D. melanogaster and its sister species (Begun et al, 2007), and comprehending their genotype-phenotype map (Hoffmann et al, 1990;Turelli and Hoffmann, 1995;Lazzaro et al, 2004Lazzaro et al, , 2006Scott et al, 2011;Zhu et al, 2012;Ventura et al, 2013). Finally, individually wild-collected flies have provided valuable information in describing and quantifying natural variants (Clark et al, 1994;Nunes et al, 2008), characterizing ecological and evolutionary dynamics of natural populations Bergland et al, 2014;Rajpurohit et al, 2017), estimating the spread dynamics of endosymbionts in natural populations (Kriesner et al, 2013), contrasting or validating laboratory results (Macdonald, 2004;Mathur and Schmidt, 2017) and testing high throughput re-sequencing techniques .…”