A Population Genomic Investigation of Immune Cell Diversity and Phagocytic Capacity in a Butterfly

Abstract

Insects rely on their innate immune system to successfully mediate complex interactions with their internal microbiota, as well as the microbes present in the environment. Given the variation in microbes across habitats, the challenges to respond to them are likely to result in local adaptations in the immune system. Here we focus upon phagocytosis, a mechanism by which pathogens and foreign particles are engulfed in order to be contained, killed, and processed. We investigated the phenotypic and genetic variation related to phagocytosis in two allopatric populations of the butterfly Pieris napi. Populations were found to differ in their hemocyte composition and overall phagocytic capability, driven by the increased phagocytic propensity of each cell type. Yet, genes annotated to phagocytosis showed no large genomic signal of divergence. However, a gene set enrichment analysis on significantly divergent genes identified loci involved in glutamine metabolism, which recently have been linked to immune cell differentiation in mammals. Together these results suggest that heritable variation in phagocytic capacity arises via a quantitative trait architecture with variation in genes affecting the activation and/or differentiation of phagocytic cells, suggesting them as potential candidate genes underlying these phenotypic differences.

Humoral and Cellular Defense Mechanisms in Rebel Workers of Apis mellifera

“…The following parameters were determined in the hemolymph samples: Phagocytic index, according to Watson et al [ 1 ] modified by Keehnen et al [ 2 ] method. To investigate the presence of phagocytic cells, a 10 µL suspension of heat-killed Escherichia coli (Sigma-Aldrich, Poznań, Poland; E. coli K-12 strain) in Luria–Bertani medium (A&A Biotechnology, Gdańsk, Poland) was added to 10 uL fresh hemolymph.…”

“…The following parameters were determined in the hemolymph samples: − Phagocytic index, according to Watson et al [1] modified by Keehnen et al [2] method.…”

“…Most proteins from hemolymph are produced in fat body cells, which also secrete antimicrobial peptides and constitute an important component of the humoral defense. In contrast, hemocytes are involved in cellular defense mechanisms, such as phagocytosis and wound repair [ 1 , 2 ]. Recent studies have shown that hemocytes are divided into those that circulate in the insect’s hemolymph and those that do not circulate, the so-called sessile hemocytes [ 3 ].…”

Population genomics reveals variable patterns of immune gene evolution in monarch butterflies (Danaus plexippus)

“…In addition to considering alternative defences, future studies on immune system evolution should also broaden the scope of the genes under investigation. For example, a recent study investigated local immune adaptation of P. napi populations in Spain and Sweden (Keehnen et al, 2021). While these populations varied strongly in phagocytic capacity, the authors did not find evidence for differential molecular evolution of phagocytosis-related genes.…”

Editorial: “Evolutionary Genetics of Insect Innate Immunity”

“…These dynamic processes shape their immune response based on the habitat they occupy. The work by Keehnen et al reports results on how the basic immune mechanism of phagocytosis may differ genetically and phenotypically between two Pieris napi allopatric populations [ 1 ]. The authors describe that indeed, the types of hemocytes and their phagocytic capacity were distinct in the two butterfly populations.…”