Evolutionary transitions to cooperative societies in fishes revisited

Abstract

Unravelling the evolution of complex social organization in animals is an important aim, not least because it helps to understand the evolutionary roots of human sociality. Recent advances in comparative methods allow to approach this question in a phylogenetic context. The validity of such comparative approaches depends strongly on the quality of information regarding the behaviour, sociality, and reproduction of animals in natural systems, and on the quality of the phylogenetic reconstruction. Applying a novel comparative approach, a recent study of Dey et al. (, Nature Ecology & Evolution, 1, 137) concluded that evolutionary transitions to cooperative breeding in cichlid fishes were not associated with the social mating pattern. Here we argue that this result was adversely affected by equivocal classifications of mating patterns, and inadequate phylogenetic data. In order to illustrate the impact of the mating system misclassifications, we scored mating patterns as reported in the original literature and re‐analysed the dataset based on Dey et al.’s tree topology. The result suggests that the mating system does in fact significantly explain the evolutionary transition to cooperative breeding in lamprologine cichlids, but we submit that a reliable conclusion cannot be reached before improving the behavioural information and the underlying phylogenetic reconstruction. The problems identified in this case study are not unique and we urge caution in the interpretation of results from comparative phylogenetic studies in general. We do agree with Dey et al. () though that the lamprologine cichlids of Lake Tanganyika may constitute a fundamental test case for the theory of social evolution, but better information on their behaviour and phylogenetic relationships is needed to allow meaningful analyses.

Insufficient data render comparative analyses of the evolution of cooperative breeding mere speculation: A reply to Dey et al.

“…Referring to our reanalysis of Dey et al's () approach, Dey et al () state “The results put forth by Tanaka et al () emerge only under the extreme scenario in which all cooperative breeding species are classified as non‐monogamous, which we argue arises because Tanaka et al () confound social systems and mating systems. … in Tanaka et al's () classification scheme, all 21 cooperatively breeding species are classified as monogamous [sic; in fact, this should read non‐monogamous] (including the 13 cooperatively breeding species in their Table 1, and the 8 additional cooperatively breeding species for which we agree on the mating system classification)”. This is an interesting comment.…”

“…Dey et al () claim to have “demonstrated that transitions to cooperative breeding in Lamprologine cichlids were not related to a species’ social mating system ” in their previous study of these fishes (Dey et al, ). They assert that our challenge of this conclusion (Tanaka et al, ) was unjustified. By focussing on the most important points of their critique, we here explain why this allegation is unfounded.…”

“…In this context, Dey et al () accuse Tanaka et al () of an assertion that in fact has not been made: “Tanaka et al claim on a re‐analysis of the data that transitions to cooperative breeding are promoted by non‐monogamous (promiscuous) breeding systems”. This allegation illustrates the central misunderstanding in this debate.…”

“…This allegation illustrates the central misunderstanding in this debate. The aim of Tanaka et al's () reanalyses was explicitly not to draw alternative conclusions on the effect of mating systems on the evolution of cooperative breeding in lamprologine cichlids. Instead, the intention was merely to illustrate the severe problem inherent in drawing conclusions from the application of comparative methods to a dubious data base.…”

“…Instead, the intention was merely to illustrate the severe problem inherent in drawing conclusions from the application of comparative methods to a dubious data base. For this very reason, Tanaka et al () remarked in the Abstract: “In order to illustrate the impact of the mating system misclassifications, we scored mating patterns as reported in the original literature and re‐analysed the dataset based on Dey et al's tree topology. The result suggests that the mating system does in fact significantly explain the evolutionary transition to cooperative breeding in lamprologine cichlids, but we submit that a reliable conclusion cannot be reached before improving the behavioural information and the underlying phylogenetic reconstruction”.…”