Origin and the elaboration of a major evolutionary transition in individuality

This topic fits nicely the theme of gene-environment interactions — the “environmental signal” is the life cycle of Camponotini (ant tribe containing two extinct genera and eight extant genera — including the carpenter ant); the “response to the signal” is the symbiotic decision (during evolution) of Biochmannia bacteria to join the ant in an obligate endosymbiosis relationship [“obligate” means that either the endosymbiont or the host cannot survive without the other (e.g. gutless marine worms of the genus Riftia which get nutrition from their endosymbiotic bacteria); the most common examples of obligate endosymbiosis are mitochondria in animal cells and chloroplasts in plant cells] — which is believed to have contributed to the ecological and evolutionary success of these two organisms. This might also be called a form of “adaptation.” Obligate endosymbiosis (in which distantly related species integrate to form a single replicating individual) represents a major evolutionary transition in individuality of an animal or plant.

Phylogenetic evidence suggests that the ancestor of Blochmannia was horizontally transferred from hemipteran bugs (a distantly related order of insects) to the most recent common ancestor of the Camponotini ~51 million years ago(!!). Blochmannia enhances nutrition by increasing amino acid synthesis, which can regulate the size of worker ants; ants, in turn, provide Blochmannia with a protected cellular environment for proliferation and to ensure strict vertical transmission of these bacteria through the germline. Consequently, Blochmannia and Camponotini have co-evolved and their phylogenies are congruent [see Fig. 4a of attached article as an excellent illustration of this evolutionary convergence].

In ants, wasps and flies, the germplasm is a maternally inherited region of cytoplasm — localized to the posterior pole of oocytes and freshly laid eggs — where it has a dual function in specifying the germline and the embryonic posterior. The mRNAs and/or proteins of a group of highly conserved ‘germline genes’ are localized together in the germplasm. To investigate whether integration of Blochmannia into Camponotini influences the germplasm, authors [see attached article] first determined the localization of mRNAs or proteins of germline genes in freshly laid eggs of Lasius niger (an early-branching species that is in the same subfamily as the Camponotini, but that lacks Blochmannia); in L. niger, authors found that three germline genes localize in a single germplasm at the posterior pole (similar to other ants, wasps and flies). These three germline genes in Camponotus floridanus (a species in Camponotini having germplasm surrounded by Blochmannia), also localized in a single germplasm at the posterior pole in oocytes.

However — as the oocyte transitioned to a freshly laid egg — nine germline genes (mRNAs or proteins) localized in one of four subcellular locations (which authors named “zones 1, 2, 3 and 4”) [see paper for details of these zones]. At a later stage, after the egg cellularizes and has initiated zygotic expression (the cellular blastoderm stage), the products of these nine genes persisted in these four zones. In both freshly laid and later-stage eggs, localization and expression of mRNAs or proteins of germline genes is combinatorial — most are present in all four zones, but nos mRNA is only in two zones, and osk mRNA is only in one zone. Moreover, localization of these mRNAs or proteins is also dynamic (in later-stage eggs, the number of zones in which nos mRNA is present increases to three, and to two for osk mRNA — but the number of zones in which smaug mRNA is present decreases from four to three). This combinatorial and dynamic localization shows that these four zones are not identical and suggests that they have distinct roles in integrating Blochmannia into the ant tissues during embryogenesis; because the freshly laid egg is a single host cell, evolution of these four distinct zones is the result of changes in the subcellular localization of maternally inherited mRNAs and proteins.

Authors therefore provided evidence for the origin and elaboration of developmental integration between Blochmannia and Camponotini in a phylogenetic tree (see Fig. 4b of attached article]. In step 1 (pre-existing capacity), a novel zone (zone 3) evolved to have a role in embryonic patterning — before the origin of this developmental integration; this event led to a pre-existing capacity to localize mRNAs and proteins into novel subcellular locations, which was subsequently co-opted to facilitate integration of Blochmannia into the Camponotini.

The Hox genes Abdominal A (abdA) and Ultrabithorax (Ubx) — which, in arthropods, normally function to differentiate abdominal and thoracic segments after they form — were rewired in the Camponotini also to regulate germline genes early in development. Consequently, the mRNAs and proteins of these Hox genes are expressed maternally and colocalize at a subcellular level with those of germline genes in the germplasm and three novel locations in the freshly laid egg. Blochmannia bacteria then selectively regulate these mRNAs and proteins to make each of these four locations functionally distinct — creating a system of coordinates in the embryo in which each location performs a different function to integrate Blochmannia into the Camponotini (!!). 😊


Nature 10 Sept 2020; 585: 239-244

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