Abstract

Among major vertebrate groups, ray-finned fishes (Actinopterygii) collectively display a nearly unrivaled diversity of parental care activities. This fact, coupled with a growing body of phylogenetic data for Actinopterygii, makes these fishes a logical model system for analyzing the evolutionary histories of alternative parental care modes and associated reproductive behaviors. From an extensive literature review, we constructed a supertree for ray-finned fishes and used its phylogenetic topology to investigate the evolution of several key reproductive states including type of parental care (maternal, paternal, or biparental), internal versus external fertilization, internal versus external gestation, nest construction behavior, and presence versus absence of sexual dichromatism (as an indicator of sexual selection). Using a comparative phylogenetic approach, we critically evaluate several hypotheses regarding evolutionary pathways toward parental care. Results from maximum parsimony reconstructions indicate that all forms of parental care, including paternal, biparental, and maternal (both external and internal to the female reproductive tract) have arisen repeatedly and independently during ray-finned fish evolution. The most common evolutionary transitions were from external fertilization directly to paternal care and from external fertilization to maternal care via the intermediate step of internal fertilization. We also used maximum likelihood phylogenetic methods to test for statistical correlations and contingencies in the evolution of pairs of reproductive traits. Sexual dichromatism and nest construction proved to be positively correlated with the evolution of male parental care in species with external fertilization. Sexual dichromatism was also positively correlated with female-internal fertilization and gestation. No clear indication emerged that female-only care or biparental care were evolutionary outgrowths of male-only care, or that biparental care has been a common evolutionary stepping stone between paternal and maternal care. Results are discussed in the context of prior thought about the evolution of alternative parental care modes in vertebrates.

Highlights

  • The males of certain fishes do all the work, and afterward take exclusive charge of the young

  • Such observations suggest that the evolutionary pathways toward parental care might differ between lineages with internal versus external syngamy

  • Many ray-finned fishes exhibit phenotypic manifestations of sexual selection, most often in the form of sexual dichromatism (Reimchen 1989; Houde and Endler 1990; Stott and Poulin 1996; Amundsen and Forgren 2001). This affords an opportunity to examine the possible role of sexual selection in the evolution of various forms of parental care in ray-finned fishes

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Summary

Introduction

The males of certain fishes do all the work, and afterward take exclusive charge of the young. Some actinopterygiian lineages have evolved highly derived parental care traits such as placental viviparity (Reznick et al 2002), male pregnancy (Berglund et al 1986; Jones and Avise 1997), and mouthbrooding (Koblmuller et al 2004) Such diversity makes the ray-finned fishes a natural model system for studying general patterns and processes of vertebrate parental care evolution (Amundsen 2003). Because gestation and internal fertilization presumably require elaborate suites of physiological, anatomical, and behavioral adaptations (Amoroso 1968; Schindler and Hamlett 1993), phylogenetic constraints and trade-offs may be important in the evolution of this form of parental care Such observations suggest that the evolutionary pathways toward parental care might differ between lineages with internal versus external syngamy. This affords an opportunity to examine the possible role of sexual selection (via its observable surrogate, sexual dichromatism) in the evolution of various forms of parental care in ray-finned fishes

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