Convergent evolution of alternative developmental trajectories associated with diapause in African and South American killifish

Andrew I. Furness, David N. Reznick, Mark S. Springer, Robert Meredith

Research output: Contribution to journalArticleResearchpeer-review

38 Citations (Scopus)

Abstract

Annual killifish adapted to life in seasonally ephemeral water-bodies exhibit desiccation resistant eggs that can undergo diapause, a period of developmental arrest, enabling them to traverse the otherwise inhospitable dry season. Environmental cues that potentially indicate the season can govern whether eggs enter a stage of diapause mid-way through development or skip this diapause and instead undergo direct development. We report, based on construction of a supermatrix phylogenetic tree of the order Cyprinodontiformes and a battery of comparative analyses, that the ability to produce diapause eggs evolved independently at least six times within African and South American killifish. We then show in species representative of these lineages that embryos entering diapause display significant reduction in development of the cranial region and circulatory system relative to directdeveloping embryos. This divergence along alternative developmental pathways begins mid-way through development, well before diapause is entered, during a period of purported maximum developmental constraint (the phylotypic period). Finally, we show that entering diapause is accompanied by a dramatic reduction in metabolic rate and concomitant increase in long-term embryo survival. Morphological divergence during the phylotypic period thus allows embryos undergoing diapause to conserve energy by shunting resources away from energetically costly organs thereby increasing survival chances in an environment that necessitates remaining dormant, buried in the soil and surrounded byan eggshell formuch of the year.Our results indicate that adaptation to seasonal aquatic environments in annual killifish imposes strong selection during the embryo stage leading to marked diversification during this otherwise conserved period of vertebrate development.

Original languageEnglish
Article number20142189
Pages (from-to)1-9
Number of pages9
JournalProceedings of the Royal Society B: Biological Sciences
Volume282
Issue number1802
DOIs
StatePublished - 28 Jan 2015

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Fundulidae
convergent evolution
diapause
African Americans
trajectories
Embryonic Structures
trajectory
Trajectories
Eggs
embryo
embryo (animal)
Soils
Water
Cyprinodontiformes
Egg Shell
egg
Desiccation
Aptitude
Body Water
Cardiovascular System

Keywords

  • Adaptation
  • Annual life cycle
  • Cyprinodontiformes

Cite this

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abstract = "Annual killifish adapted to life in seasonally ephemeral water-bodies exhibit desiccation resistant eggs that can undergo diapause, a period of developmental arrest, enabling them to traverse the otherwise inhospitable dry season. Environmental cues that potentially indicate the season can govern whether eggs enter a stage of diapause mid-way through development or skip this diapause and instead undergo direct development. We report, based on construction of a supermatrix phylogenetic tree of the order Cyprinodontiformes and a battery of comparative analyses, that the ability to produce diapause eggs evolved independently at least six times within African and South American killifish. We then show in species representative of these lineages that embryos entering diapause display significant reduction in development of the cranial region and circulatory system relative to directdeveloping embryos. This divergence along alternative developmental pathways begins mid-way through development, well before diapause is entered, during a period of purported maximum developmental constraint (the phylotypic period). Finally, we show that entering diapause is accompanied by a dramatic reduction in metabolic rate and concomitant increase in long-term embryo survival. Morphological divergence during the phylotypic period thus allows embryos undergoing diapause to conserve energy by shunting resources away from energetically costly organs thereby increasing survival chances in an environment that necessitates remaining dormant, buried in the soil and surrounded byan eggshell formuch of the year.Our results indicate that adaptation to seasonal aquatic environments in annual killifish imposes strong selection during the embryo stage leading to marked diversification during this otherwise conserved period of vertebrate development.",
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Convergent evolution of alternative developmental trajectories associated with diapause in African and South American killifish. / Furness, Andrew I.; Reznick, David N.; Springer, Mark S.; Meredith, Robert.

In: Proceedings of the Royal Society B: Biological Sciences, Vol. 282, No. 1802, 20142189, 28.01.2015, p. 1-9.

Research output: Contribution to journalArticleResearchpeer-review

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