Organ-specific patterns of endopolyploidy in the giant ant Dinoponera australis

Abstract

Endoreduplication is an alternative cell cycle that omits cell division such that cellular ploidy increases, generating "endopolyploidy". Endoreduplication is common among eukaryotes and is thought to be important in generalized cell differentiation. Previous research on ants suggests that they endoreduplicate in body segment-dependent manners. In this study, we measured endopolyploidy of specific organs within ant body segments to determine which organs are driving these segment-specific patterns and whether endopolyploidy is related to organ function. We dissected fourteen organs from each of five individuals of Dinoponera australis and measured endopolyploidy of each organ via flow cytometry. Abdominal organs had higher levels of endopolyploidy than organs from the head and thorax, driven by particularly high ploidy levels for organs with digestive or exocrine function. In contrast, organs of the reproductive, muscular, and neural systems had relatively low endopolyploidy. These results provide insight into the segment-specific patterns of endopolyploidy previously reported and into the specific organs that employ endoreduplication in their functional development. Future work aimed at quantifying the metabolic and gene expression effects of endoreduplication will clarify how this often overlooked genomic event contributes to the development and function of specialized organs across the breadth of taxa that are known to endoreduplicate.

Comparative physiology of Malpighian tubules: form and function

“…9 In Dinoponera australis, organs related to digestion and excretion present the much higher levels of endopolyploidy when compared with other organs such as brain and muscle. 31 This was also observed in Apis mellifera by Rangel et al, 32 although no statistically significant differences were observed. In addition to differences with regard to other organs, in Apis mellifera, MT showed higher ploidy values in an age-dependent manner.…”

Endopolyploidy as a potential driver of animal ecology and evolution

“…As has been previously shown in plants (Nagl, ; Barow & Meister, ; Edgar et al ., ), endopolyploid levels in animals also feature taxon‐ and tissue‐specific variation (Table ). In at least some invertebrates, a large fraction of somatic cells may be polyploid (Scholes et al ., ), although the degree of endopolyploidy can itself be influenced by internal (e.g. age, nutritional status) and external (e.g.…”

“…In arthropods (e.g. hymenopterans), endopolyploid levels can reach 512C across tissues such as Malpighian tubules, small intestine, and thoracic gland (Scholes et al ., ), and salivary glands routinely achieve endopolyploid levels of 1024C or more (Nagl, ). The neurons of molluscs feature remarkable ploidy variation, from a modest 32C in the land snail Triodopsis divesta to an astounding 200000C in the gigantic neurons of the sea hare Aplysia californica (Lasek & Dower, ; Mandrioli et al ., ).…”

Evolutionary relationship of fat body endoreduplication and queen fecundity in termites

“…Endoreduplication is often attributed to increasing cellular size, metabolism, and gene expression owing to the increasing availability of DNA templates for transcription (Bourdon et al, ; Claycomb, Benasutti, Bosco, Fenger, & Orr‐Weaver, ; Edgar et al, ; Galitski, Saldanha, Styles, Lander, & Fink, ; Nagl, ). In social hymenopterans, several studies have shown the intriguing linkage between caste specialization and endopolyploidy (Rangel, Strauss, Seedorf, Hjelmen, & Johnston, ; Scholes, Suarez, & Paige, ; Scholes, Suarez, Smith, Johnston, & Paige, ). Scholes et al () investigated the degree of polyploidy within and among castes of four ant species with worker polymorphism and observed variation in ploidy levels among workers with different body sizes.…”