Male ants disguised by the queen's bouquet

Abstract

Males of the tropical ant Cardiocondyla obscurior are either wingless and aggressive or winged and docile, and both compete for access to virgin queens in the nest^1,2. Although the fighter males (ergatoids) attack and kill other ergatoids, they tolerate and even attempt to mate with their winged rivals. Here we show that the winged males avoid the aggression of wingless males by mimicking the chemical bouquet of virgin queens, but that their mating success is not reduced as a result. This example of female mimicry by vigorous males is surprising, as in other species it is typically used as a protective strategy by weaker males, and may explain the coexistence and equal mating success of two male morphs.

Main

Ants typically mate during short nuptial flights that give little opportunity for male–male combat³. By contrast, sexual individuals of C. obscurior mate inside their natal nests. Intensive intrasexual competition has led to the evolution of sabre-shaped mandibles and escalated fighting to the death among locally mating ergatoid males^1,2. Winged males, on the other hand, have weak mandibles, behave peacefully and leave the nest one to two weeks after emergence in order to mate outside. But, surprisingly, before dispersal they are as successful as ergatoid males in attaining copulations with virgin nestmate queens (U-test: U = 903.0, P = 0.86, n_ergatoid = 33 observations for 24 min each, n_winged = 56). Ergatoid males would therefore be expected to benefit from killing their winged rivals⁴.

Contrary to the aggression that might be expected towards winged males, ergatoid males typically restrict their fighting to other ergatoids, and attempt to mate with the winged males¹. Our behavioural observations indicate that young winged males (1–5 days old) are as attractive as young virgin queens to ergatoid males (ergatoid males mounted 11 out of 12 winged males and 15 out of 17 virgin queens; 72–120 min observation per individual; Fisher's exact test: d.f. = 1, P = 1.0). By contrast, ergatoid males showed no interest in older winged males (6–10 days, n = 17; old–young: P < 0.001), whereas virgin queens remained attractive regardless of their age (old: 12 out of 14; old–young: P = 1.0).

This toleration of winged males and attempts at homosexual mating with them can be explained by the chemical resemblance of winged males and virgin queens in their bouquet of cuticular hydrocarbons on the body surface, which are important for communication in social insects^5,6,7,8. In a discriminant analysis of hydrocarbon profiles obtained by gas chromatography with mass spectrometry⁹, 1-day-old winged males and virgin queens formed a single cluster that was distinct from those of ergatoid males and workers (Fig. 1a). However, for 10-day-old ants, all four groups were clearly separated (Fig. 1b). We conclude that the odour similarity of young — and only young — winged males to virgin queens explains their age-dependent attractiveness to ergatoid males.

Figure 1: Discriminant analysis of the hydrocarbon profiles of 1-day-old (filled symbols) and 10-day-old (hollow symbols) Cardiocondyla obscurior ants.

Hydrocarbons were extracted from workers (day 1: n₁ = 10, day 10: n₁₀ = 10; circles), ergatoid males (n₁ = 13, n₁₀ = 12; squares), winged males (n₁ = 14, n₁₀ = 8; diamonds) and virgin queens (n₁ = 13, n₁₀ = 7; triangles) by gas chromatography with mass spectrometry, and were statistically analysed by principal-components analysis followed by stepwise discriminant analysis¹³. Results show the first two canonical discriminant functions (percentage of variability is shown in parentheses). a, One-day-old ants: virgin queens and winged males cluster together but are distinct from ergatoid males and workers (81.6% of individuals classified correctly; F1: Wilks' λ = 0.018, P < 0.001; F2: Wilks' λ = 0.194, P < 0.005). b, Ten-day-old ants: all colony members form distinct groups (as the non-plotted third significant function discriminates workers and ergatoid males; 100% of individuals classified correctly; F1: Wilks' λ = 0.001, P < 0.001; F2: Wilks' λ = 0.023, P < 0.001).

Most examples of chemical deception occur between species⁵, whereas intraspecific female mimicry is typically based on morphological or behavioural similarities¹⁰. Chemical female mimicry occurs in male rove beetles¹¹ and garter snakes¹² when they find themselves in adverse physiological conditions. These males pay for avoiding competition with 'high-quality' males by suffering low mating success with females. By contrast, in Cardiocondyla, the odour mimicry of virgin queens by young winged males does not affect their copulatory success when compared to older, non-mimicking winged males (U = 324.0, P = 0.30, n_young = 25, n_old = 31) and ergatoid males (U = 393.0, P = 0.76).

Cardiocondyla provides a new evolutionary context for chemical deception: it is deployed irrespective of condition by all young winged males and renders them simultaneously attractive to both sexes. This example of chemical female mimicry enables two alternative reproductive strategies to exist in the male sex.