Environmental osmolality influences sperm motility activation in an anuran amphibian

Byrne, Phillip G.; Dunne, Craig; Munn, Adam J.; Silla, Aimee J.

doi:10.1111/jeb.12584

Cited by 19 publications

(31 citation statements)

References 71 publications

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“…For organisms with external fertilization, eggs and sperm are exposed to the ambient environment, and hence, fertilization and early development are influenced by external environmental factors such as pH and salinity (Holliday 1969;Sayer et al 1993;Nissling et al 2002;Havenhand et al 2008;Allen and Pechenik 2010;Byrne et al 2015). Local adaptation of reproductive traits results in reduced gene flow as a by-product.…”

mentioning

confidence: 99%

Immigrant reproductive dysfunction facilitates ecological speciation

et al. 2017

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The distributions of species are not only determined by where they can survive - they must also be able to reproduce. Although immigrant inviability is a well-established concept, the fact that immigrants also need to be able to effectively reproduce in foreign environments has not been fully appreciated in the study of adaptive divergence and speciation. Fertilization and reproduction are sensitive life-history stages that could be detrimentally affected for immigrants in non-native habitats. We propose that "immigrant reproductive dysfunction" is a hitherto overlooked aspect of reproductive isolation caused by natural selection on immigrants. This idea is supported by results from experiments on an externally fertilizing fish (sand goby, Pomatoschistus minutus). Growth and condition of adults were not affected by non-native salinity whereas males spawning as immigrants had lower sperm motility and hatching success than residents. We interpret these results as evidence for local adaptation or acclimation of sperm, and possibly also components of paternal care. The resulting loss in fitness, which we call "immigrant reproductive dysfunction," has the potential to reduce gene flow between populations with locally adapted reproduction, and it may play a role in species distributions and speciation.

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mentioning

confidence: 99%

Immigrant reproductive dysfunction facilitates ecological speciation

et al. 2017

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“…Manier & Palumbi ; Byrne et al . ). Gene flow among populations could then be reduced either via direct viability selection against immigrants (Nosil et al .…”

Section: The Missing Component: Intraspecific Variationmentioning

confidence: 97%

“…Moreover, also sperm may be under divergent natural selection (e.g. Manier & Palumbi 2008;Byrne et al 2015). Gene flow among populations could then be reduced either via direct viability selection against immigrants (Nosil et al 2005;Hangartner et al 2012)mediated by differential embryonic performanceor due to the disruption of locally adapted (sperm and egg) genotype combinations (Findlay & Swanson 2009;Nosil 2012).…”

Section: The Missing Component: Intraspecific Variationmentioning

confidence: 99%

Evolution of egg coats: linking molecular biology and ecology

2015

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One central goal of evolutionary biology is to explain how biological diversity emerges and is maintained in nature. Given the complexity of the phenotype and the multifaceted nature of inheritance, modern evolutionary ecological studies rely heavily on the use of molecular tools. Here, we show how molecular tools help to gain insight into the role of egg coats (i.e. the extracellular structures surrounding eggs and embryos) in evolutionary diversification. Egg coats are maternally derived structures that have many biological functions from mediating fertilization to protecting the embryo from environmental hazards. They show great molecular, structural and functional diversity across species, but intraspecific variability and the role of ecology in egg coat evolution have largely been overlooked. Given that much of the variation that influences egg coat function is ultimately determined by their molecular phenotype, cutting-edge molecular tools (e.g. proteomics, glycomics and transcriptomics), combined with functional assays, are needed for rigorous inferences on their evolutionary ecology. Here, we identify key research areas and highlight emerging molecular techniques that can increase our understanding of the role of egg coats in the evolution of biological diversity, from adaptation to speciation.

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“…At ejaculation, sperm motility activates instantly on contact with an appropriate external medium (plain fresh or salt water in most documented cases). A substantial chemical change in the fertilizing environment requires either (i) post‐ejaculated sperm swimming performance to evolve via natural selection so that populations have sperm locally adapted to their environments (this has been demonstrated on a fine scale in the frog Crinia signifera (Byrne, Dunne, Munn, & Silla, 2015), and the sand goby Pomatoschistus minutus (Svensson et al., 2017)), or (ii) individuals to migrate for reproduction. Although diadromous fishes migrate across marine and freshwater habitats (catadromous salt water spawn, fresh water growth; anadromous fresh water spawn, salt water growth), they must return to their natal environment for spawning because typically marine fish sperm activate upon hypertonic shock with sea water (no activation in fresh water), whereas freshwater fish (and amphibian) sperm activate upon hypotonic shock or decrease in specific ions (Alavi & Cosson, 2006; Browne et al., 2015; Cosson, 2010).…”

Section: Introductionmentioning

confidence: 99%

A novel sperm adaptation to evolutionary constraints on reproduction: Pre‐ejaculatory sperm activation in the beach spawning capelin (Osmeridae)

Beirão

Lewis

Wringe

et al. 2018

Ecology and Evolution

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Reproduction of external fertilizing vertebrates is typically constrained to either fresh or salt water, not both. For all studied amphibians and fishes, this constraint includes immotile sperm that are activated after ejaculation only by the specific chemistry of the fertilizing medium in which the species evolved (fresh, brackish, or salt water). No amphibians can reproduce in the sea. Although diadromous fishes may migrate between salt and fresh water, they are shackled to their natal environment for spawning in part because of sperm activation. Here, we report for the first time among all documented external fertilizing vertebrates, that in the absence of any external media, sperm are motile at ejaculation in a marine spawning fish (Osmeridae, capelin, Mallotus villosus). To illuminate why, we evaluated sperm behavior at different salinities in M. villosus as well as the related freshwater spawning anadromous rainbow smelt (Osmerus mordax). Surprisingly, sperm performance was superior in fresh water for both species. M. villosus spend their entire life at sea but our results show that their sperm are deactivated by sea water, suggesting a freshwater ancestry. By circumventing constraining water chemistry, we interpret the unique pre‐ejaculatory sperm activation in this species as a novel adaptation that enables fertilization in the marine environment. These findings also contribute to understanding the persistence of anadromy, despite great energetic costs to adult fishes.

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Environmental osmolality influences sperm motility activation in an anuran amphibian

Cited by 19 publications

References 71 publications

Immigrant reproductive dysfunction facilitates ecological speciation

Immigrant reproductive dysfunction facilitates ecological speciation

Evolution of egg coats: linking molecular biology and ecology

A novel sperm adaptation to evolutionary constraints on reproduction: Pre‐ejaculatory sperm activation in the beach spawning capelin (Osmeridae)

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