Worker reproduction of the invasive yellow crazy ant Anoplolepis gracilipes

Abstract

Background: Reproductive division of labor is one of the key features of social insects. Queens are adapted for reproduction while workers are adapted for foraging and colony maintenance. In many species, however, workers retain functional ovaries and can lay unfertilized male eggs or trophic eggs. Here we report for the first time on the occurrence of physogastric workers and apparent worker reproduction in the invasive yellow crazy ant Anoplolepis gracilipes (Fr. Smith). We further examined the reproductive potential and nutritional role of physogastric workers through multidisciplinary approaches including morphological characterization, laboratory manipulation, genetic analysis and behavioral observation.

Results: Egg production with two types of eggs, namely reproductive and trophic eggs, by physogastric workers was found. The reproductive egg was confirmed to be haploid and male-destined, suggesting that the workers produced males via arrhenotokous parthenogenesis as no spermatheca was discovered. Detailed observations suggested that larvae were mainly fed with trophic eggs. Along with consumption of trophic eggs by queens and other castes as part of their diet, the vital role of physogastric workers as "trophic specialist" is confirmed.

Conclusion: We propose that adaptive advantages derived from worker reproduction for A. gracilipes may include 1) trophic eggs provisioned by physogastric workers likely assist colonies of A. gracilipes in overcoming unfavorable conditions such as paucity of food during critical founding stage; 2) worker-produced males are fertile and thus might offer an inclusive fitness advantage for the doomed orphaned colony.

Keywords: Anoplolepis gracilipes; arrhenotokous parthenogenesis; physogastric workers; trophic eggs.

Fig. 1

Morphology and reproductive systems in worker and queen of A. gracilipes. Shown are the external morphology of normal worker (a), physogastric worker (b) and queen (c). Gaster dissection presenting ovarian morphology of normal worker (d), physogastric worker (e) and queen (f). Note difference in length of ovarioles and number of mature oocytes

Fig. 2

Scanning electron micrographs and histological sections of two types of workers in A. gracilipes. SEMs of abdomen of normal worker (a) and physogastric worker (b), and longitudinal sections through posterior abdomen part of normal worker (c) and physogastric worker (d). Note large accumulation of fat body and absence of spermatheca in physogastric worker. The location where spermatheca is supposed to be found if it exists is highlighted with circled area in figure (e). DGd: Dufour gland duct, FB: fat body, HG: hindgut, MT: Malpighian tubules, OV: ovaries, OVD: oviduct, VG: venom gland, VGd: venom gland duct

Fig. 3

Morphology of eggs produced by A. gracilipes workers. Light micrograph of a worker-laid reproductive egg (a) and a worker-laid trophic egg (b)

Fig. 4

Morphological comparison between worker-produced and queen-produced offspring in A. gracilipes. a Male pupa from orphaned colony (left), worker pupa (middle) and male pupa from queenright colony (right); (b) external morphology of worker-produced male (left) and normal queen-produced male (right); (c) close up of external genital structure of worker-produced male (left) and queen-produced male (right); (d) internal organs of the male reproductive system of worker-produced male (left) and queen-produced male (right)