Population genetic analysis of autophagy and phagocytosis genes in Drosophila melanogaster and D. simulans

Joo Hyun Im,Brian P Lazzaro,Arnar Palsson

doi:10.1371/journal.pone.0205024

Abstract

Autophagy and phagocytosis are cellular immune mechanisms for internalization and elimination of intracellular and extracellular pathogens. Some pathogens have evolved the ability to inhibit or manipulate these processes, raising the prospect of adaptive reciprocal co-evolution by the host. We performed population genetic analyses on phagocytosis and autophagy genes in Drosophila melanogaster and D. simulans to test for molecular evolutionary signatures of immune adaptation. We found that phagocytosis and autophagy genes as a whole exhibited an elevated level of haplotype homozygosity in both species. In addition, we detected signatures of recent selection, notably in the Atg14 and Ykt6 genes in D. melanogaster and a pattern of elevated sequence divergence in the genderblind (gb) gene on the D. simulans lineage. These results suggest that the evolution of the host cellular immune system as a whole may be shaped by a dynamic conflict between Drosophila and its pathogens even without pervasive evidence of strong adaptive evolution at the individual gene level.

Highlights

Phagocytosis is a primary cellular immune process in Drosophila [1]
To examine whether autophagy and phagocytosis genes exhibit any signature of recent positive selection, we calculated the following summary statistics for each focal gene and its corresponding control genes: Watterson’s estimator, Tajima’s D (TajD), normalized Fay and Wu’s H, Ewens-Watterson’s homozygosity (EW), and the compound test statistic DHEW
To determine whether the combined group of all autophagy and phagocytosis genes shows evidence of recent selection or recurrent adaptive evolution, we explored whether the population genetic statistics of these genes are statistically significantly different from their respective control genes by calculating the mean of comparison scores for each focal-control gene pairing for each statistic (Table 1)

Summary

Introduction

Phagocytosis is a primary cellular immune process in Drosophila [1]. During phagocytosis, extracellular pathogens are recognized by opsonins and phagocytic receptors, engulfed at the host membrane, and internalized and degraded in compartments called phagosomes [2] (Fig 1). Intracellular bacteria and viruses are encapsulated by isolation membranes called phagosphores, which are nucleated and expanded to form autophagosomes to destroy the pathogen [4, 5] (Fig 1). Both phagosomes and autophagosomes are eventually fused with a lysosome to degrade internalized pathogens [6]. When phagocytosis fails to eliminate pathogens due to modification or damage to the phagosome by bacteria, autophagy works as a back-up process to overcome infection [9, 10]

Methods

Results

Conclusion