Parasite defensive limb movements enhance acoustic signal attraction in male little torrent frogs

Abstract

Many animals rely on complex signals that target multiple senses to attract mates and repel rivals. These multimodal displays can however also attract unintended receivers, which can be an important driver of signal complexity. Despite being taxonomically widespread, we often lack insight into how multimodal signals evolve from unimodal signals and in particular what roles unintended eavesdroppers play. Here, we assess whether the physical movements of parasite defense behavior increase the complexity and attractiveness of an acoustic sexual signal in the little torrent frog (Amolops torrentis). Calling males of this species often display limb movements in order to defend against blood-sucking parasites such as frog-biting midges that eavesdrop on their acoustic signal. Through mate choice tests we show that some of these midge-evoked movements influence female preference for acoustic signals. Our data suggest that midge-induced movements may be incorporated into a sexual display, targeting both hearing and vision in the intended receiver. Females may play an important role in incorporating these multiple components because they prefer signals which combine multiple modalities. Our results thus help to understand the relationship between natural and sexual selection pressure operating on signalers and how in turn this may influence multimodal signal evolution.

Keywords: Amolops torrentis; ecology; evolutionary biology; mate choice; multimodal communication; natural selection; parasite; pre-existing bias.

Figure 1.. Diagrammatic drawings of seven limb motion displays shown by male little torrent frogs.

Figure 2.. The proportion of different limb displays and the correlation between parasites and limb displays.

(A) The distribution ratio of parasite-induced and spontaneous displays in each limb movement (N=69 males). TT, toe trembling; HFL, hind foot lifting; AW, arm waving; LSA, limb shaking; W, wiping. The numbers in brackets above each bar pairs represent the number of each movement, showing the richness of those visual displays. (B) The relationship between parasite stress and the number of all limb movements (N=39 males). Black circles represent different individuals recorded in the field.

Figure 3.. Photos of frogs being bitten by potential parasites.

Figure 4.. Calling males (N=39) show more parasite-evoked limb movements than silent males (N=30).

AW, arm waving; W, wiping; LSA, limb shaking; HFL, hind foot lifting. ^*p < 0.05, ^***p < 0.001. Black circles represent the extreme values of each group.

Figure 5.. Female choices in (A) AW versus control, (B) HFL versus control, (C) W versus control, and (D) LSA versus control.

All limb display videos are accompanied by advertisement call and male movement, while the controls contain the same call and frog but in absence of limb movement. AW, arm waving; HFL, hind foot lifting; W, wiping; LSA, limb shaking. ^*p < 0.05. ns, not statistically significant.

Figure 6.. Transitional matrix between three behavioral units shown by male little torrent frogs.

Call, AW, and HFL represent advertisement call, arm waving, and hind foot lifting, respectively. Numbers next to lines and arrows indicate the transitional probabilities.

Figure 7.. Differences between close-range group (N=4) and long-range group (N=39) in the number of male frogs that have the LS + FF movement (A) and the frequency of LS + FF display (B).

LS, leg stretching; FF, foot flagging. ^**p < 0.01, ^***p < 0.001. Black circles in part B represent the extreme values of long-distance group.

Figure 8.. Schematic of the acoustic and visual playback arena.

The picture of the female frog represents the initial placement point for each playback test.