Vestigial preference functions in neural networks and túngara frogs

Abstract

Although there is a growing interest in understanding how perceptual mechanisms influence behavioral evolution, few studies have addressed how perception itself is shaped by evolutionary forces. We used a combination of artificial neural network models and behavioral experiments to investigate how evolutionary history influenced the perceptual processes used in mate choice by female túngara frogs. We manipulated the evolutionary history of artificial neural network models and observed an emergent bias toward calls resembling known ancestral states. We then probed female túngara frogs for similar preferences, finding strong biases toward stimuli that resemble a call hypothesized for a recent ancestor. The data strongly suggest that female túngara frogs exhibit vestigial preferences for ancestral calls, and provide a general strategy for exploring the role of historical contingency in perceptual biases.

Figure 1

(a) Mimetic and mirrored histories in acoustic space defined by two dimensions of a principal components analysis (see refs. and 36). Open circles represent the calls of extant and “ancestral” taxa. The shaded area is used in subsequent figures. (b) Sonograms of signals used in mimetic and mirrored histories. Root calls are at bottom of sequence, túngara at top. Each sonogram is 600 msec long (x axis), and spans from 0 to 1.5 kHz (y axis).

Figure 2

Schematic depiction of hypotheses for network preference functions. (a) Mimetic history network exhibiting vestigial preferences. (b) Mirrored history network exhibiting vestigial preferences. (c) Null hypothesis of no historical influence for both mimetic and mirrored history networks. The upper row depicts isoclines of preferences in the principal-component space given in Fig. 1. Lower row depicts hypothesized preferences varied in a single dimension, time to half frequency, which loads highly on principal component 1 (PC1).

Figure 3

Vestigial preference functions in mimetic and mirrored history networks. (a) Sonograms of calls with a time to half frequency (THHz) 1 SD smaller than, equal to, or 1 SD greater than the túngara frog call (left to right). Each sonogram is 600 ms long (x axis), and spans from 0 to 1.5 kHz (y axis). (b) Mimetic history networks (filled circles) exhibit preferences for steep whines resembling their ancestors. Responses of mirrored networks are shown in open circles for comparison. (c) Mirrored history networks (gray circles) exhibit preferences for shallow whines resembling their ancestors. Mimetic network responses are plotted in open circles.

Figure 4

(a) Schematic depicting vestigial-preference hypothesis for túngara frog females. Note that ancestral calls are defined as positive, and so lie on the right of the túngara frog call. (b) Responses of female túngara frogs to ancestral and anti-ancestral calls in recognition tests. Dashed line represents criterion for a significantly recognized call. Horizontal lines indicate recognition responses that were significantly different from one another (P < 0.01). (c) Responses of female túngara frogs to ancestral and anti-ancestral calls in discrimination tests. Filled bars represent responses to ancestral stimuli; gray bars responses to anti-ancestral stimuli. Horizontal line depicts null hypothesis of no preference.