TY - JOUR

T1 - Orphan gene in Littorina

T2 - An unexpected role of symbionts in the host evolution

AU - Maltseva, A. L.

AU - Lobov, A. A.

AU - Pavlova, P. A.

AU - Panova, M.

AU - Gafarova, E. R.

AU - Marques, J. P.

AU - Danilov, L. G.

AU - Granovitch, A. I.

N1 - Publisher Copyright: © 2022 Elsevier B.V.

PY - 2022/5/25

Y1 - 2022/5/25

N2 - Mechanisms of reproductive isolation between closely related sympatric species are of high evolutionary significance as they may function as initial drivers of speciation and protect species integrity afterwards. Proteins involved in the establishment of reproductive barriers often evolve fast and may be key players in cessation of gene flow between the incipient species. The five Atlantic Littorina (Neritrema) species represent a notable example of recent radiation. The geographic ranges of these young species largely overlap and the mechanisms of reproductive isolation are poorly understood. In this study, we performed a detailed analysis of the reproductive protein LOSP, previously identified in Littorina. We showed that this protein is evolutionary young and taxonomically restricted to the genus Littorina. It has high sequence variation both within and between Littorina species, which is compatible with its presumable role in the reproductive isolation. The strongest differences in the LOSP structure were detected between Littorina subgenera with distinctive repetitive motifs present exclusively in the Neritrema species, but not in L. littorea. Moreover, the sequence of these repetitive structural elements demonstrates a high homology with genetic elements of bacteria, identified as components of Littorina associated microbiomes. We suggest that these elements were acquired from a symbiotic bacterial donor via horizontal genetic transfer (HGT), which is indirectly confirmed by the presence of multiple transposable elements in the LOSP flanking and intronic regions. Furthermore, we hypothesize that this HGT-driven evolutionary innovation promoted LOSP function in reproductive isolation, which might be one of the factors determining the intensive cladogenesis in the Littorina (Neritrema) lineage in contrast to the anagenesis in the L. littorea clade.

AB - Mechanisms of reproductive isolation between closely related sympatric species are of high evolutionary significance as they may function as initial drivers of speciation and protect species integrity afterwards. Proteins involved in the establishment of reproductive barriers often evolve fast and may be key players in cessation of gene flow between the incipient species. The five Atlantic Littorina (Neritrema) species represent a notable example of recent radiation. The geographic ranges of these young species largely overlap and the mechanisms of reproductive isolation are poorly understood. In this study, we performed a detailed analysis of the reproductive protein LOSP, previously identified in Littorina. We showed that this protein is evolutionary young and taxonomically restricted to the genus Littorina. It has high sequence variation both within and between Littorina species, which is compatible with its presumable role in the reproductive isolation. The strongest differences in the LOSP structure were detected between Littorina subgenera with distinctive repetitive motifs present exclusively in the Neritrema species, but not in L. littorea. Moreover, the sequence of these repetitive structural elements demonstrates a high homology with genetic elements of bacteria, identified as components of Littorina associated microbiomes. We suggest that these elements were acquired from a symbiotic bacterial donor via horizontal genetic transfer (HGT), which is indirectly confirmed by the presence of multiple transposable elements in the LOSP flanking and intronic regions. Furthermore, we hypothesize that this HGT-driven evolutionary innovation promoted LOSP function in reproductive isolation, which might be one of the factors determining the intensive cladogenesis in the Littorina (Neritrema) lineage in contrast to the anagenesis in the L. littorea clade.

KW - Cryptic species

KW - Horizontal genetic transfer

KW - Littorina

KW - Orphan-gene

KW - Reproductive protein

KW - Reproductive Isolation

KW - Microbiota

KW - Animals

KW - Gene Flow

KW - Genetic Speciation

KW - Bacteria

KW - Snails/genetics

KW - BACTERIA

KW - GASTROPODA

KW - PROTEIN

KW - MECHANISMS

KW - ORIGIN

KW - FAUNA

KW - MULTIPLE PATERNITY

KW - SYMPATRIC SPECIATION

KW - DIVERGENCE

UR - http://www.scopus.com/inward/record.url?scp=85126287637&partnerID=8YFLogxK

U2 - 10.1016/j.gene.2022.146389

DO - 10.1016/j.gene.2022.146389

M3 - Article

C2 - 35257790

AN - SCOPUS:85126287637

VL - 824

JO - Gene

JF - Gene

SN - 0378-1119

M1 - 146389

ER -