Thelytokous parthenogenesis in the fungus-gardening ant Mycocepurus smithii (Hymenoptera: Formicidae)

Abstract

The general prevalence of sexual reproduction over asexual reproduction among organisms testifies to the evolutionary benefits of recombination, such as accelerated adaptation to changing environments and elimination of deleterious mutations. Documented instances of asexual reproduction in groups otherwise dominated by sexual reproduction challenge evolutionary biologists to understand the special circumstances that might confer an advantage to asexual reproductive strategies. Here we report one such instance of asexual reproduction in the ants. We present evidence for obligate thelytoky in the asexual fungus-gardening ant, Mycocepurus smithii, in which queens produce female offspring from unfertilized eggs, workers are sterile, and males appear to be completely absent. Obligate thelytoky is implicated by reproductive physiology of queens, lack of males, absence of mating behavior, and natural history observations. An obligate thelytoky hypothesis is further supported by the absence of evidence indicating sexual reproduction or genetic recombination across the species' extensive distribution range (Mexico-Argentina). Potential conflicting evidence for sexual reproduction in this species derives from three Mycocepurus males reported in the literature, previously regarded as possible males of M. smithii. However, we show here that these specimens represent males of the congeneric species M. obsoletus, and not males of M. smithii. Mycocepurus smithii is unique among ants and among eusocial Hymenoptera, in that males seem to be completely absent and only queens (and not workers) produce diploid offspring via thelytoky. Because colonies consisting only of females can be propagated consecutively in the laboratory, M. smithii could be an adequate study organism a) to test hypotheses of the population-genetic advantages and disadvantages of asexual reproduction in a social organism and b) inform kin conflict theory.For a Portuguese translation of the abstract, please see Abstract S1.

Figure 1. Spatial distribution of nest entrances and fungus chambers of the studied Mycocepurus smithii population.

Nest entrances are depicted as Xs, queenright chambers as solid black dots and all other fungus chambers as open black circles; size of circles does not represent the relative sizes of nest chambers. The x and y axes are labeled in cm. The nest excavation was continued 50 cm beyond the study plot limits in all four directions and no additional chambers were found.

Figure 2. Internal reproductive organs of Mycocepurus smithii (A, B) and M. goeldii queens (C, D) in reflecting light (A, C) and transmission light (B, D).

Arrows drawn from the top left to the bottom right point to the spermatheca and arrows drawn from the top right to the bottom left point to yellow bodies. (A, B) The spermatheca of M. smithii is translucent (empty), the ovaries are developed and yellow bodies are present. (C, D) A reproductively active M. goeldii queen has an opaque, sperm-filled spermatheca, developed ovaries and yellow bodies. The scale bar represents 2 mm in all images.

Figure 3. Morphological comparison of one of the Mycocepurus males collected by W. Kerr in Rio Claro in 1960 (A, B, C) and a Mycocepurus obsoletus male (D, E, F).

(A) lateral view of ‘Kerr male’, (B) forewing and (C) hindwing in dorsal view. (D) Male of Mycocepurus obsoletus in lateral view, (E) forewing and (F) hindwing in dorsal view. Morphological characters informative for species identification are the shape of the propodeal spine, of the petiole and the wing venation. Scale bars represents 1 mm in all images.

Figure 4. Geographic distribution of Mycocepurus obsoletus.

Thick black lines depict the boundaries of Brazilian States, open circles represent collections based on worker specimens, the solid black dot depicts the collection site of the ‘Kerr males’: Rio Claro in São Paulo Sate. From north to south, M. obsoletus has been recorded in the States of Pará, Tocantins, Goiás, the Federal District, Minas Gerais and São Paulo. Besides Rio Claro, M. obsoletus has been collected in two other localities in São Paulo Sate: a) Reserva Ecológica de Jataí near Luis Antônio (23–25.V.1997, Silvestre & Silva col.; see [35]), which is located approximately 100 km north of Rio Claro, and b) Ibitinga (25.I.1964, K. Lenko col.), which is approximately 150 km northwest of Rio Claro.