For the road: calibrated maternal investment in light of extracellular symbiont transmission

Abstract

Faithful transmission of beneficial symbionts is critical for the persistence of mutualisms. Many insect groups rely on extracellular routes that require microbial symbionts to survive outside the host during transfer. However, given a prolonged aposymbiotic phase in offspring, how do mothers mitigate the risk of symbiont loss due to unsuccessful transmission? Here, we investigated symbiont regulation and reacquisition during extracellular transfer in the tortoise beetle, Chelymorpha alternans (Coleoptera: Cassidinae). Like many cassidines, C. alternans relies on egg caplets to vertically propagate its obligate symbiont Candidatus Stammera capleta. On average, each caplet is supplied with 12 symbiont-bearing spheres where Stammera is embedded. We observe limited deviation (±2.3) in the number of spheres allocated to each caplet, indicating strict maternal control over symbiont supply. Larvae acquire Stammera 1 day prior to eclosion but are unable to do so after hatching, suggesting that a specific developmental window governs symbiont uptake. Experimentally manipulating the number of spheres available to each egg revealed that a single sphere is sufficient to ensure successful colonization by Stammera relative to the 12 typically packaged within a caplet. Collectively, our findings shed light on a tightly regulated symbiont transmission cycle optimized to ensure extracellular transfer.

Maternal provisioning of an obligate symbiont

“…By quantifying the number and size of larvae from H. panicea as well as the number of bacteria and ‘ Ca . H. symbioticus,’ we reject the hypothesis that the offspring of this viviparous sponge are vertically transmitted a similar number of obligate symbionts [5, 8–10]. H. panicea appears to take an alternative strategy: a maternal pool of ‘ Ca .…”

“…Evolutionary ecology is centered around the examinations of individual life-history characters, of which are increasingly recognized to be dependent on microbial symbionts [51–54]. Provided that holobionts are units of biological organization upon which multilevel selection acts [55, 56], the ways that mothers impact offspring survival, performance, and fitness is anticipated to include the microbes that associate with the offspring [1–3, 5, 35, 48, 57, 58]. Our quantitative estimates of H. panicea reproduction and ‘ Ca .…”

“…symbioticus is presumed to be adaptive [25][26][27] and is possibly part of a bet-hedging strategy to maximize maternal fitness in an unpredictable environment, such as that of the Baltic Sea [5,7,27,31,35,[48][49][50].…”

“…A threshold in symbiont quantity is often required to ensure that these partnerships are maintained through the developmental stages [1][2][3][4]. This minimum can span six orders of magnitude (from 10s to >1 million) and can incur an inter-sibling variability of less than 20% [5][6][7][8][9]. The aphid Uroleucon ambrosiae, for example, provides ~10 3 (± ~5%) cells of the nutritional mutualist Buchnera spp.…”

“…to each egg, while the stinkbug Megacopta punctatissima produces one capsule with ~10 8 cells of the obligate symbiont Candidatus Ishikawaella capsulate for every 3 to 4 eggs [9,10]. This interpretation of vertical transmission-that all offspring within a clutch of any fecundity are provided a similar number of symbionts [1][2][3][4]-stems primarily from oviparous insects [5,[8][9][10] and, thus, has yet to consider other major reproductive strategies.…”