Reproductive Mode and Conflict Shape the Evolution of Male Attributes and Rate of Speciation in the Fish Family Poeciliidae

Abstract

Sexual conflict is caused by differences between the sexes in how fitness is maximized. These differences are shaped by the discrepancy in the investment in gametes, how mates are chosen and how embryos and young are provided for. Fish in the family Poeciliidae vary from completely provisioning eggs before they are fertilized to providing virtually all resources after fertilization via the functional equivalent of a mammalian placenta. This shift in when females provision their young relative to when an egg is fertilized is predicted to cause a fundamental change in when and how sexual conflict is manifested. If eggs are provisioned before fertilization, there should be strong selection for females to choose with whom they mate. Maternal provisioning after fertilization should promote a shift to post-copulatory mate choice. The evolution of maternal provisioning may in turn have cascading effects on the evolution of diverse features of the biology of these fish because of this shift in when mates are chosen. Here we summarize what these consequences are and show that the evolution of maternal provisioning is indeed associated with and appears to govern the evolution of male traits associated with sexual selection. The evolution of placentas and associated conflict does not cause accelerated speciation, contrary to predictions. Accelerated speciation rate is instead correlated with the evolution of male traits associated with sexual selection, which implies a more prominent role of pre-copulatory reproductive isolation in causing speciation in this family.

Male reproductive phenotype and coercive mating performance in the guppyPoecilia reticulata

“…To the best of our knowledge, our study on guppies and that of Head et al 2015 on mosquitofish are the only attempts so far to examine relationships between multiple male traits and their combinations and coercive mating success. Although coercion is the most common male mating behavior observed in this fish family and the exclusive mating tactic in approximately half of the species (Reznick et al 2021), most attention has been directed towards the role of female choice on the evolution of male reproductive phenotype (Evans et al 2011a). Our understanding of the strength and shape of sexual selection on male phenotypes associated with gonopodial thrusting is therefore still very limited, in particular for species in which males can adopt both tactics opportunistically.…”

Increased superfetation precedes the evolution of advanced degrees of placentotrophy in viviparous fishes of the family Poeciliidae

“…Here is where other selective mechanisms must have been the main driving forces of placentation. In particular, elaborate placentas provide females with greater control over the amount and type of nutrients that are allocated to each embryo, which is critical in the context of intergenomic ( parent-offspring) conflict [15,18,38]. This is the central idea behind the viviparity-driven conflict hypothesis, which also attempts to explain the evolution of placentotrophy [39,40].…”

The Evolution of Alternative Buoyancy Mechanisms in Freshwater Fish Eggs

“…Although the buoyancy of a majority of perciform fishes is lower, the reproductive pattern for most of these fishes is of aphrophils, with eggs deposited in bubble nests, which typically comprise a floating raft of mucous foam that keeps the eggs at the surface while guarded by a parent (Balon, 1975;Hostache and Mol, 1998;Wootton and Smith, 2015). These egg buoyancy adaptations suggest the evolution of ARTs in contrasting biotopes, which potentially contributes to reproductive isolation (Taylor, 1999;Funk et al, 2006;Reznick et al, 2021).…”