Sex-specific perceptual spaces for a vertebrate basal social aggregative behavior

Abstract

Loose aggregations of fishes, or shoals, are a basal social organization of vertebrates and offer a valuable opportunity to determine how individual perceptions influence group formation. We used zebrafish, Danio rerio, to comprehensively investigate the preference space for shoaling related to adult pigment pattern variation, presented in the form of 17 zebrafish pigment pattern mutants or closely related species. We examined all combinations of these phenotypes in 2,920 initial and replicated preference tests, and used as subjects both domesticated laboratory stocks and wild-caught fish. By using multidimensional scaling and other approaches, we show that laboratory and wild zebrafish exhibit similar preferences, yet, unexpectedly, these preferences differ markedly between sexes, and also from how human observers perceive the same pigment patterns. Whereas zebrafish males respond to two traits (species and stripe patterning) in deciding whether to join a shoal, zebrafish female preferences do not correlate with a priori identifiable traits, and neither perceptual world is correlated with that of human observers. The observed zebrafish sex differences run counter to the most commonly accepted explanations for the individual selective advantages gained by shoaling. More generally, these data describe very different perceptual worlds between sexes and reveal the importance of sex differences in social group formation, as well as the critical importance of defining species specificity in visual signaling.

Fig. 1.

Diverse pigment patterns of zebrafish (Left and Center) and closely related species (Right). Abbreviations: A, albino mutant; C, csf1r mutant; CE, csf1r, ednrb1 double mutant; CK, csf1r, kit double mutant; DI, dali/+ mutant; DU, duchamp/+ mutant; E, ednrb1 mutant; K, kit mutant; M, mitfa mutant; O, oberon mutant; S, seurat mutant; Da, Danio albolineatus; Dc, D. choprae; Dk, D. aff. kyathit; Dn, D. nigrofasciatus; Ds, Devario shanensis. For simplicity, only phenotype abbreviations are used in the text and figures. For additional information on the genetic bases of mutant phenotypes and species differences, see refs. –.

Fig. 2.

Male shoaling preference increases with vertical pattern entropy of pigment pattern relative to WT when alternative phenotypes are presented simultaneously with WT. Shown are differences in the times spent with each phenotype (abbreviations in Fig. 1) compared with WT, plotted against differences in vertical pattern entropy compared with WT. Red line, regression for zebrafish mutants; yellow line, regression for other species; diamond, relative position for WT stimulus shoals; other symbols are alternative stimulus shoals. Circles, zebrafish mutants; squares, Other species; open symbols denote uniform pigment patterns; filled symbols indicate the presence of spots; symbols bisected horizontally denote horizontal stripes; symbols bisected vertically denote vertical bars.

Fig. 3.

MDS solutions for perceptual spaces of humans, male zebrafish, and female zebrafish. Abbreviations and symbols are as in Figs. 1 and 2, respectively. (A) MDS recovers intuitive groupings of stimulus phenotypes from similarity rankings by human subjects. MDS solution: R² = 0.67; stress (a lack-of-fit measure; refs. and 30), s = 0.22. (B and C) Shoaling preference spaces for male (B) and female (C) zebrafish differ dramatically from one another and from human perceptions of these phenotypes. (B) MDS solution for zebrafish males: R² = 0.51; s = 0.27. (C) MDS solution for zebrafish females: R² = 0.52; s = 0.26.