Stocktake Sale on now: wide range of books at up to 70% off!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

Evidence of mitochondrial capture in Australian glass shrimp (Paratya australiensis) in south-eastern Queensland

Sharmeen Rahman https://orcid.org/0000-0003-4826-3566 A B * , Daniel J. Schmidt A B and Jane M. Hughes A B
+ Author Affiliations
- Author Affiliations

A School of Environment and Science, Griffith University, Brisbane, Qld 4111, Australia.

B Australian Rivers Institute, Griffith University, Brisbane, Qld 4111, Australia.


Handling Editor: Peter Unmack

Marine and Freshwater Research 73(8) 1098-1106 https://doi.org/10.1071/MF21304
Submitted: 15 October 2021  Accepted: 8 June 2022   Published: 18 July 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context: The Australian glass shrimp (Paratya australiensis) has been identified as a cryptic species complex and several lineages occur sympatrically in eastern Australia. In south-eastern Queensland, the predominant lineages are ‘4’ and ‘6’, although the only known area of sympatry in the Conondale Range is the result of a translocation.

Aim: Our aim was to determine any evidence of natural sympatry between the two lineages in the Mary River catchment area using polymerase chain reatction–restriction fragment length polymorphism (PCR-RFLP) analysis.

Methods: Of six sites sampled, only one site showed sympatry between Lineage 4 and 6, so 39 individuals from this site were sequenced using fragment of the mtDNA COI gene and a neighbour joining tree revealed the existence of two lineages.

Results: On the basis of two sets of nuclear markers (allozymes and microsatellites), there was no evidence of two species, because all loci conformed to Hardy–Weinberg expectations and only Lineage 4 alleles were identified.

Conclusion: These results led to the inference that the existence of two mtDNA lineages could be due to mitochondrial capture.

Implication: The current situation in the Broken Bridge High site could be due to historical interbreeding between the two lineages reflected in the mtDNA data but not evident in the nuclear data.

Keywords: cryptic species, freshwater shrimp, historical interbreeding, hybridisation, lineages, mitochondrial DNA, nuclear DNA, sympatry.


References

Allendorf FW, Luikart G, Aitken SN (2012) ‘Conservation and the genetics of populations.’ (Wiley)

Andersen, MJ, McCullough, JM, Gyllenhaal, EF, Mapel, XM, Haryoko, T, Jønsson, KA, and Joseph, L (2021). Complex histories of gene flow and a mitochondrial capture event in a nonsister pair of birds. Molecular Ecology 30, 2087–2103.
Complex histories of gene flow and a mitochondrial capture event in a nonsister pair of birds.Crossref | GoogleScholarGoogle Scholar | 33615597PubMed |

Avise JC (2000) ‘Phylogeography: the history and formation of species.’ (Harvard University Press: Cambridge, MA, USA)

Bickford, D, Lohman, DJ, Sodhi, NS, Ng, PKL, Meier, R, Winker, K, Ingram, KK, and Das, I (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22, 148–155.
Cryptic species as a window on diversity and conservation.Crossref | GoogleScholarGoogle Scholar |

Cook, BD, Baker, AM, Page, TJ, Grant, SC, Fawcett, JH, Hurwood, DA, and Hughes, JM (2006). Biogeographic history of an Australian freshwater shrimp, Paratya australiensis (Atyidae): the role life history transition in phylogeographic diversification. Molecular Ecology 15, 1083–1093.
Biogeographic history of an Australian freshwater shrimp, Paratya australiensis (Atyidae): the role life history transition in phylogeographic diversification.Crossref | GoogleScholarGoogle Scholar | 16599968PubMed |

Cook, BD, Bunn, SE, and Hughes, JM (2007). A comparative analysis of population structuring and genetic diversity in sympatric lineages of freshwater shrimp (Atyidae: Paratya): concerted or independent responses to hydrographic factors? Freshwater Biology 52, 2156–2171.
A comparative analysis of population structuring and genetic diversity in sympatric lineages of freshwater shrimp (Atyidae: Paratya): concerted or independent responses to hydrographic factors?Crossref | GoogleScholarGoogle Scholar |

Crandall, KA, Bininda-Emonds, ORP, Mace, GM, and Wayne, RK (2000). Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution 15, 290–295.
Considering evolutionary processes in conservation biology.Crossref | GoogleScholarGoogle Scholar |

Dasmahapatra, KK, Elias, M, Hill, RI, Hoffman, JI, and Mallet, J (2010). Mitochondrial DNA barcoding detects some species that are real, and some that are not. Molecular Ecology Resources 10, 264–273.
Mitochondrial DNA barcoding detects some species that are real, and some that are not.Crossref | GoogleScholarGoogle Scholar | 21565021PubMed |

Excoffier, L, and Lischer, HEL (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar | 21565059PubMed |

Fawcett, JH, Hurwood, DA, and Hughes, JM (2010). Consequences of a translocation between two divergent lineages of the Paratya australiensis (Decapoda: Atyidae) complex: reproductive success and relative fitness. Journal of the North American Benthological Society 29, 1170–1180.
Consequences of a translocation between two divergent lineages of the Paratya australiensis (Decapoda: Atyidae) complex: reproductive success and relative fitness.Crossref | GoogleScholarGoogle Scholar |

Fedorov, VB, Trucchi, E, Goropashnaya, AV, and Stenseth, NC (2022). Conflicting nuclear and mitogenome phylogenies reveal ancient mitochondrial replacement between two North American species of collared lemmings (Dicrostonyx groenlandicus, D. hudsonius). Molecular Phylogenetics and Evolution 168, 107399.
Conflicting nuclear and mitogenome phylogenies reveal ancient mitochondrial replacement between two North American species of collared lemmings (Dicrostonyx groenlandicus, D. hudsonius).Crossref | GoogleScholarGoogle Scholar | 35026429PubMed |

Folmer, O, Black, M, Hoeh, W, Lutz, R, and Vrijenhoek, R (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 7881515PubMed |

Garzon TR (2009) Hybridization between closely related lineages in the Paratya australiensis (Decapoda: Atyidae) species complex. PhD dissertation, Griffith University, Qld, Australia.

Good, JM, Hird, S, Reid, N, Demboski, JR, Steppan, SJ, Martin-Nims, TR, and Sullivan, J (2008). Ancient hybridization and mitochondrial capture between two species of chipmunks. Molecular Ecology 17, 1313–1327.
Ancient hybridization and mitochondrial capture between two species of chipmunks.Crossref | GoogleScholarGoogle Scholar | 18302691PubMed |

Hancock, MA, and Hughes, J (1999). Direct measures of instream movement in a freshwater shrimp using a genetic marker. Hydrobiologia 416, 23–32.
Direct measures of instream movement in a freshwater shrimp using a genetic marker.Crossref | GoogleScholarGoogle Scholar |

Hughes, JM, Bunn, SE, Kingston, DM, and Hurwood, DA (1995). Genetic differentiation and dispersal among populations of Paratya australiensis (Atyidae) in rainforest streams in southeast Queensland, Australia. Journal of the North American Benthological Society 14, 158–173.
Genetic differentiation and dispersal among populations of Paratya australiensis (Atyidae) in rainforest streams in southeast Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |

Hughes, J, Goudkamp, K, Hurwood, D, Hancock, M, and Bunn, S (2003). Translocation causes extinction of a local population of the freshwater shrimp Paratya australiensis. Conservation Biology 17, 1007–1012.
Translocation causes extinction of a local population of the freshwater shrimp Paratya australiensis.Crossref | GoogleScholarGoogle Scholar |

Hurwood, DA, Hughes, JM, Bunn, SE, and Cleary, C (2003). Population structure in the freshwater shrimp (Paratya australiensis) inferred from allozymes and mitochondrial DNA. Heredity 90, 64–70.
Population structure in the freshwater shrimp (Paratya australiensis) inferred from allozymes and mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 12522427PubMed |

Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P, and Drummond, A (2012). Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar | 22543367PubMed |

Leys, M, Keller, I, Räsänen, K, Gattolliat, J-L, and Robinson, CT (2016). Distribution and population genetic variation of cryptic species of the Alpine mayfly Baetis alpinus (Ephemeroptera: Baetidae) in the Central Alps. BMC Evolutionary Biology 16, 77.
Distribution and population genetic variation of cryptic species of the Alpine mayfly Baetis alpinus (Ephemeroptera: Baetidae) in the Central Alps.Crossref | GoogleScholarGoogle Scholar | 27068234PubMed |

Marková, S, Dufresne, F, Manca, M, and Kotlík, P (2013). Mitochondrial capture misleads about ecological speciation in the Daphnia pulex complex. PLoS ONE 8, e69497.
Mitochondrial capture misleads about ecological speciation in the Daphnia pulex complex.Crossref | GoogleScholarGoogle Scholar | 23869244PubMed |

Nei M (1987) ‘Molecular evolutionary genetics.’ (Columbia University Press: New York, NY, USA)
| Crossref |

Page, TJ, Baker, AM, Cook, BD, and Hughes, JM (2005). Historical transoceanic dispersal of a freshwater shrimp: the colonization of the South Pacific by the genus Paratya (Atyidae). Journal of Biogeography 32, 581–593.
Historical transoceanic dispersal of a freshwater shrimp: the colonization of the South Pacific by the genus Paratya (Atyidae).Crossref | GoogleScholarGoogle Scholar |

Page, TJ, von Rintelen, K, and Hughes, JM (2007). An island in the stream: Australia’s place in the cosmopolitan world of Indo-West Pacific freshwater shrimp (Decapoda: Atyidae: Caridina). Molecular Phylogenetics and Evolution 43, 645–659.
An island in the stream: Australia’s place in the cosmopolitan world of Indo-West Pacific freshwater shrimp (Decapoda: Atyidae: Caridina).Crossref | GoogleScholarGoogle Scholar | 17011796PubMed |

Perea, S, Vukić, J, Šanda, R, and Doadrio, I (2016). Ancient mitochondrial capture as factor promoting mitonuclear discordance in freshwater fishes: a case study in the genus Squalius (Actinopterygii, Cyprinidae) in Greece. PLoS ONE 11, e0166292.
Ancient mitochondrial capture as factor promoting mitonuclear discordance in freshwater fishes: a case study in the genus Squalius (Actinopterygii, Cyprinidae) in Greece.Crossref | GoogleScholarGoogle Scholar | 27906993PubMed |

Pfenninger, M, and Schwenk, K (2007). Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology 7, 121.
Cryptic animal species are homogeneously distributed among taxa and biogeographical regions.Crossref | GoogleScholarGoogle Scholar | 17640383PubMed |

Rahman, S, Schmidt, D, and Hughes, JM (2020). Genetic structure of Australian glass shrimp, Paratya australiensis, in relation to altitude. PeerJ 8, e8139.
Genetic structure of Australian glass shrimp, Paratya australiensis, in relation to altitude.Crossref | GoogleScholarGoogle Scholar | 31942250PubMed |

Real, KM, Schmidt, DJ, and Hughes, JM (2009). Mogurnda adspersa microsatellite markers: multiplexing and multi-tailed primer tagging. Conservation Genetics Resources 1, 411.
Mogurnda adspersa microsatellite markers: multiplexing and multi-tailed primer tagging.Crossref | GoogleScholarGoogle Scholar |

Rogl K (2021) A genomics perspective of species and speciation in an Atyid shrimp (Paratya australiensis) PhD dissertation, Queensland University of Technology, Qld, Australia.

Rozas, J, Ferrer-Mata, A, Sánchez-DelBarrio, JC, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE, and Sánchez-Gracia, A (2017). DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34, 3299–3302.
DnaSP 6: DNA sequence polymorphism analysis of large data sets.Crossref | GoogleScholarGoogle Scholar | 29029172PubMed |

Wang, B, and Wang, X-R (2014). Mitochondrial DNA capture and divergence in Pinus provide new insights into the evolution of the genus. Molecular Phylogenetics and Evolution 80, 20–30.
Mitochondrial DNA capture and divergence in Pinus provide new insights into the evolution of the genus.Crossref | GoogleScholarGoogle Scholar | 25106134PubMed |

Werle, E, Schneider, C, Renner, M, Völker, M, and Fiehn, W (1994). Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Research 22, 4354–4355.
Convenient single-step, one tube purification of PCR products for direct sequencing.Crossref | GoogleScholarGoogle Scholar | 7937169PubMed |

Wilson, JD, Schmidt, DJ, and Hughes, JM (2016). Movement of a hybrid zone between lineages of the Australian glass shrimp (Paratya australiensis). Journal of Heredity 107, 413–422.
Movement of a hybrid zone between lineages of the Australian glass shrimp (Paratya australiensis).Crossref | GoogleScholarGoogle Scholar | 27225934PubMed |

Wright JL (2012) The effects of secondary contact on reproduction in closely related lineages of the freshwater shrimp Paratya australiensis (Decapoda:Atyidae). Queensland, Australia. BSc(Hons) thesis, Griffith University, Qld, Australia.