More than meets the eye: syntopic and morphologically similar mangrove killifish species show different mating systems and patterns of genetic structure along the Brazilian coast

Abstract

Different mating systems can strongly affect the extent of genetic diversity and population structure among species. Given the increased effects of genetic drift on reduced population size, theory predicts that species undergoing self-fertilisation should have greater population structure than outcrossed species; however, demographic dynamics may affect this scenario. The mangrove killifish clade is composed of the two only known examples of self-fertilising species among vertebrates (Kryptolebias marmoratus and Kryptolebias hermaphroditus). A third species in this clade, Kryptolebias ocellatus, inhabits mangrove forests in southeast Brazil; however, its mating system and patterns of genetic structure have been rarely explored. Here, we examined the genetic structure and phylogeographic patterns of K. ocellatus along its distribution, using mitochondrial DNA and microsatellites to compare its patterns of genetic structure with the predominantly selfing and often-syntopic, K. hermaphroditus. Our results indicate that K. ocellatus reproduces mainly by outcrossing, with no current evidence of selfing, despite being an androdioecious species. Our results also reveal a stronger population subdivision in K. ocellatus compared to K. hermaphroditus, contrary to the theoretical predictions based on reproductive biology of the two species. Our findings indicate that, although morphologically similar, K. ocellatus and K. hermaphroditus had remarkably different evolutionary histories when colonising the same mangrove areas in southeastern Brazil, with other factors (e.g., time of colonisation, dispersal/establishment capacity) having more profound effects on the current population structuring of those species than differences in mating systems.

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Fig. 1: Sampling locations for Kryptolebias ocellatus and K. hermaphroditus.
Fig. 2: Phylogenetic reconstruction and haplotype network for cox1 data in K. ocellatus.
Fig. 3: Genetic clusters among sampling points of K. ocellatus.

Data availability

cox1 mtDNA sequences are deposited in GenBank (accession numbers: K. ocellatus: MN400774–MN400902; K. hermaphroditus: MN400903–MN400963). Microsatellite genotypes are available at Dryad Digital Repository: https://doi.org/10.5061/dryad.m0cfxpp1n.

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Acknowledgements

We are grateful to ICMbio for providing help with accommodation and facilities, especially the teams working at Parque Estadual Serra do Mar: Núcleo Picinguaba and Parque Estadual Serra do Mar: Estação Ecológica Juréia-Itatins. We are thankful to Dr. Ingo Schlupp from Oklahoma University for his friendly review. We also thank Dr. Joana Robalo and two other anonymous reviewers whose comments and suggestions substantially improved the paper.

Funding

This work was supported by the National Geographic/Waitt program [W461-16] and by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) [233161/2014-7]. SMQL receives research productivity grant issued by CNPq [313644/2018-7]. AT is grateful for support from the funds provided by the University of California at Irvine to Prof. John C. Avise. HMVE-S received a postdoctoral fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES).

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SC, WMB-F, AT, SMQL and CGL conceived the study and obtained the funding. WMB-F, HMVE-S, MGL and SMQL collected the samples. WMB-F and AT carried out the genetic analyses. WMB-F wrote the paper with participation of all authors.

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Correspondence to Waldir M. Berbel-Filho.

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This work followed the Swansea ethics committee guidelines (SU-Ethics-Student-250717/245). Sampling work was carried out under license ICMBio/SISBIO 57145-1/2017.

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Berbel-Filho, W.M., Tatarenkov, A., Espírito-Santo, H.M.V. et al. More than meets the eye: syntopic and morphologically similar mangrove killifish species show different mating systems and patterns of genetic structure along the Brazilian coast. Heredity 125, 340–352 (2020). https://doi.org/10.1038/s41437-020-00356-y

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