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Influence of the Rate of Changes in the COX1 Gene on Body Size and Sexual Selection in Carp Hybridization

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Abstract

The influence of mtDNA cytochrome c-oxidase I gene fragment variability on body length has been studied in 12 species of cyprinids, which may have hybrids with Rutilus rutilus L. and Abramis brama L., and in reciprocal hybrids (RA and AR) and alloplasmatic backcrosses (ARR and RAA) of roach (R) and bream (A). It has been established that the rate of nucleotide substitutions in COX1 is negatively related not only to body size but also to fish lifespan which differentiates them into two groups: group I (species with a high rate of COX1 changes and a relatively small body size) and group II (species with low sequence variability and relatively large body size). The boundary for the distinguished groups runs between species of the same genus, Leuciscus leuciscus and L. idus: with a twofold decrease in the rate of substitutions in ide, a twofold increase in body size and lifespan occurs, which indicates a decrease in the rate of cellular respiration and free radical leak, and the exact mitonuclear match respiratory complexes. Presumably, the decrease in the rate of COX1 changes in species of group II and in bleak Alburnus alburnus is associated with an increase in the size of the genome, which provides the additional protection of genes from chemical mutagens and, regardless of body size, reduces the rate of aerobic metabolism. It has been experimentally shown that mtDNA affects body length. When bream mtDNA is included in the roach nuclear genome, ARR backcrosses have the body length of a bream and high viability, while RAA backcrosses with roach mtDNA and the bream nuclear genome inherit the roach body length and reduce viability. Species of group II are not able to effectively use the highly polymorphic mtDNA of species of group I, which is also manifested by a violation of the inheritance of a longer bream body length in RA hybrids and leads to reproductive isolation. Group I species, such as Rutilus rutilus, can include mtDNA of both groups in their genome, which underlies sexual selection in hybridization. Accordingly, sexual size dimorphism has a genetic origin, and the body size for a potential partner can be a signal for determining the mitonuclear compatibility of genomes in respiratory complexes.

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ACKNOWLEDGMENTS

We express deep gratitude and appreciation to Yu.V. Slynko (Institute of Biology of Inland Waters, Russian Academy of Sciences (RAS)) for the guidance in the study of hybrids; S.K. Semenova, R.I. Ludanny, and G.N. Khrisanfova (Institute of Gene Biology, RAS) for training and consultations, Yu.V. Kodukhova and V.V. Pavlova (Institute of Biology of Inland Waters, RAS) for cooperation; and N.V. Ovchinnikova, E.N. Pakunova, and E.I. Lavrova for assistance in carrying out work on the Sunoga pond farm of the Institute of Biology of Inland Waters, RAS.

Funding

This work was supported by the Program of the Presidium of the Russian Academy of Sciences “Wildlife: Current State and Problems of Development” as part of State Tasks no. 121050500046-8 and no. 121051100104-6 “Biodiversity, Structure, and Functioning of Freshwater Fish in Continental Reservoirs and Streams.”

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Stolbunova, V.V., Borovikova, E.A. Influence of the Rate of Changes in the COX1 Gene on Body Size and Sexual Selection in Carp Hybridization. Inland Water Biol 16, 1098–1111 (2023). https://doi.org/10.1134/S199508292306024X

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