Desiccated desert locust embryos reserve yolk as a "lunch box" for posthatching survival

Abstract

Oviparous animals often prioritize the allocation of reproductive resources to egg size over clutch size, but the impact of this maternal investment on the allocation of embryonic yolks and its ecological functions is poorly understood. We investigated how desert locust embryos allocate yolk for survival energy after hatching, rather than embryonic somatic growth depending on egg size in response to desiccation stress. Crowd-reared females (gregarious phase) produced significantly larger progeny with higher tolerance to starvation than females reared in isolation (solitarious phase). Abnormally small hatchlings with residual yolk in their gut emerged from small and large eggs when exposed to desiccation. In particular, these small hatchlings of desiccated eggs survived significantly longer under starvation than those of wet ones, with larger eggs providing even greater survival benefits. Physiological analysis showed that hatchlings from desiccated eggs showed a trade-off by reserving more lipids without somatic growth than those from normal eggs. Desiccation could be a reliable signal for embryos to predict future poor vegetation, and reserved energy could increase the chance of accessing food after hatching. Our results underscore adaptive plasticity in maternal and embryonic resource allocation in desert locusts in response to unpredictably variable semi-arid habitats.

Keywords: adaptive strategy; desiccation; embryos; maternal effects; resource allocation.

Fig. 1.

Solitarious (SOL) small and gregarious (GREG) large eggs exposed to either wet or desiccated conditions.

Fig. 2.

Hatchlings from either wet or desiccated solitarious (SOL) and gregarious (GREG) eggs. Hatchlings from desiccated eggs have yolk in the gut (arrow).

Fig. 3.

Physiological traits of fresh body weight (A), water content (B), dry body weight (C), and lipid content (D) from hatchlings from wet or desiccated solitarious (SOL) small and gregarious (GREG) large eggs of desert locusts. Each box plot displays the median value with the ends of the boxes representing the 25th and 75th percentiles, and the ends of the lines representing the 10th and 90th percentiles. Different letters above each box indicate significant differences at P < 0.05 (Tukey–Kramer HSD test). Numbers in figures indicate sample sizes.

Fig. 4.

Survival curve of hatchlings from wet (bullet, dotted line) or desiccated eggs (filled triangle, solid line) derived from solitarious small or gregarious large eggs under starvation. Numbers in figures indicate sample sizes.

Fig. 5.

A) Photographs of hatchlings, B) fresh body weight, and C) survival rate for normal wet small and large eggs and hatchlings from large eggs after yolk removal in desert locusts. Each box plot displays the median value with the ends of the boxes representing the 25th and 75th percentiles and the ends of the lines representing the 10th and 90th percentiles. Different letters above each box indicate significant differences at P < 0.05 (Tukey–Kramer HSD test). Numbers in figures indicate sample sizes.

Fig. 6.

Percentage of insects that reached second stadium after various lengths of starvation from wet solitarious small or gregarious large eggs and desiccated large eggs in desert locusts. Different letters above each circle indicate significant differences at P < 0.000368 by post hoc Fisher's exact test with Bonferroni correction. Sample sizes range from 19 to 70 at each circle.

Fig. 7.

Physiological changes in dry body weight A) and lipid content B) associated with starvation in hatchlings produced by solitarious and gregarious eggs in desert locusts. Each variable was measured pre- and poststarvation. Numbers in a figure indicate sample sizes. Each box plot displays the median value with the ends of the boxes representing the 25th and 75th percentiles, and the ends of the lines representing the 10th and 90th percentiles. Different letters above each box indicate significant differences at P < 0.05 (Tukey–Kramer HSD test). Numbers in figures indicate sample sizes.

Fig. 8.

Experimental design. Egg pods derived from isolated- or crowd-reared females are used for two treatments: either wet (control) or desiccation treatment. Crowded-reared locusts lay larger but fewer eggs than isolated-reared ones. Eggs and hatchlings derived from isolated and crowd-reared females will be termed solitarious and gregarious, respectively. Typical phenotypes of hatchlings are illustrated with their reserved yolk. Please see Materials and methods for details.