Abstract
There is increasing evidence that females can somehow improve their offspring fitness by mating with multiple males, but we understand little about the exact stage(s) at which such benefits are gained. Here, we measure whether offspring fitness is influenced by mechanisms operating solely between sperm and egg. Using externally fertilizing and polyandrous Atlantic salmon (Salmo salar), we employed split-clutch and split-ejaculate in vitro fertilization experiments to generate offspring using designs that either denied or applied opportunities for sperm competition and cryptic female choice. Following fertilizations, we measured 140 days of offspring fitness after hatch, through growth and survival in hatchery and near-natural conditions. Despite an average composite mortality of 61%, offspring fitness at every life stage was near-identical between groups fertilized under the absence versus presence of opportunities for sperm competition and cryptic female choice. Of the 21 551 and 21 771 eggs from 24 females fertilized under monandrous versus polyandrous conditions, 68% versus 67.8% survived to the 100-day juvenile stage; sub-samples showed similar hatching success (73.1% versus 74.3%), had similar survival over 40 days in near-natural streams (57.3% versus 56.2%) and grew at similar rates throughout. We therefore found no evidence that gamete-specific interactions allow offspring fitness benefits when polyandrous fertilization conditions provide opportunities for sperm competition and cryptic female choice.
Highlights
Polyandry, when females mate with multiple males within a reproductive cycle, is a predominant mating pattern [1,2,3]
Should reproductive mechanisms exist at the gamete level that allow females to harvest this potential improvement in offspring fitness by choosing the genetically ‘right’ sperm for fertilization, the question over what explains the persistence of polyandry as a natural mating pattern could be answered [28]
Following paired comparisons of offspring generated from up to 21 551 versus 21 771 eggs from up to 24 females and 16 males, we find that offspring fitness was almost identical between treatment groups that had been fertilized in the presence versus absence of opportunities for sperm competition and cryptic female choice
Summary
Polyandry, when females mate with multiple males within a reproductive cycle, is a predominant mating pattern [1,2,3]. If post-mating mechanisms exist that encourage differential fertilization success through sperm competition [12] and/or cryptic female choice [13], mating with multiple males could allow females to encourage fertilization by the ‘best’ males in the population, and gain indirect genetic benefits for their offspring. Should reproductive mechanisms exist at the gamete level that allow females to harvest this potential improvement in offspring fitness by choosing the genetically ‘right’ sperm for fertilization, the question over what explains the persistence of polyandry as a natural mating pattern could be answered [28]. Atlantic salmon females are naturally promiscuous, with microsatellite paternity measures revealing that an average of eight males, and up to 16, father a single nest in the wild [39], providing opportunities for the evolution of cryptic female choice mechanisms. Should polyandry at the level of sperm and egg allow offspring fitness benefits, our findings could improve the success of hatchery operations
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