Intergeneric hybrids inform reproductive isolating barriers in the Antarctic icefish radiation

Thomas Desvignes,Kathleen A Shusdock,Sierra S Smith,Laura C Goetz,Nathalie R Le François,John H Postlethwait,H William Detrich,Sandra K Parker

doi:10.1038/s41598-019-42354-z

Thomas Desvignes, Kathleen A Shusdock + Show 6 more

Open Access

https://doi.org/10.1038/s41598-019-42354-z

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Abstract

Interspecific hybridization or barriers to hybridization may have contributed to the diversification of Antarctic icefishes (Channichthyidae), but data supporting these hypotheses is scarce. To understand the potential for hybridization and to investigate reproductive isolating mechanisms among icefish species, we performed in vitro fertilization experiments using eggs from a female blackfin icefish Chaenocephalus aceratus and sperm from a male of another genera, the ocellated icefish Chionodraco rastrospinosus. Sequencing of genomic and mitochondrial DNA confirmed the intergeneric hybrid nature of resulting embryos which successfully developed and hatched as active larvae at about four and a half months during the Antarctic winter. This result demonstrates the compatibility of gametes of these two species and the viability of resulting zygotes and larvae. Due to logistic constraints and the slow developmental rate of icefishes, we could not test for long-term hybrid viability, fertility, fitness, or hybrid breakdown. Analysis of our fishing records and available literature, however, suggests that the strongest barriers to hybridization among parapatric icefish species are likely to be behavioral and characterized by assortative mating and species-specific courtship and nesting behaviors. This conclusion suggests that, in long-lived fish species with late sexual maturity and high energetic investment in reproduction like icefishes, pre-mating barriers are energetically more efficient than post-mating barriers to prevent hybridization.

Highlights

Icefishes have long been known by sailors and explorers of the Southern Ocean, but since the first scientific report of fish with “colorless blood” by Ditlef Rustad in 1927 and the validation in 1954 by Johan Ruud that icefishes live without hemoglobin in their blood[1], these unique fish have fascinated evolutionary biologists
C. aceratus, was exclusively captured at locations shallower than 200 m, whereas C. rastrospinosus was found within a wider bathymetric range with specimens caught as deep as 620–640 m
On the West Antarctic Peninsula (WAP), our capture data demonstrate that C. aceratus and C. rastrospinosus have partially overlapping spatial and bathymetric distributions and can be considered parapatric species

Summary

Introduction

Icefishes (or Channichthyidae) have long been known by sailors and explorers of the Southern Ocean, but since the first scientific report of fish with “colorless blood” by Ditlef Rustad in 1927 and the validation in 1954 by Johan Ruud that icefishes live without hemoglobin in their blood[1], these unique fish have fascinated evolutionary biologists. Marino et al.[33] detected signals of past genetic introgression and identified potential F1 hybrids among the three species of the icefish genus Chionodraco. No other reports have identified individual fish as hybrids between two icefish species or, between any pair of Notothenioid species. To test the possibility of hybridization and to investigate the existence of hybridization barriers in Antarctic Notothenioids, we attempted in vitro fertilization between a female blackfin icefish Chaenocephalus aceratus, a species with a sequenced genome[34], and a male ocellated icefish Chionodraco rastrospinosus. F1 hybrids were verified genetically by species-specific DNA polymorphisms To our knowledge, this is the first successful attempt to make hybrids between different genera, or even different species, of Notothenioid fish. Results impact our understanding of barriers that may reproductively isolate icefish species and contribute to species divergence

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