Contrasting patterns of genetic structure in two species of the coral trout Plectropomus (Serranidae) from east and west Australia: Introgressive hybridisation or ancestral polymorphisms

https://doi.org/10.1016/j.ympev.2006.04.024Get rights and content

Abstract

Inter-specific genetic relationships among regional populations of two species of grouper (Plectropomus maculatus and Plectropomus leopardus) were examined using mitochondrial and nuclear markers. mtDNA revealed contrasting regional inter-specific patterns whilst nuclear markers revealed contrasting patterns among markers, irrespective of region. In eastern Australia (EA) the species form a single mtDNA lineage, but the two species are reciprocally monophyletic in Western Australia (WA). This supports previous evidence for hybridisation between these species on the east coast. WA P. leopardus forms a sister relationship with the EA P. leopardus-maculatus clade while WA P. maculatus is more basal and sister to the P. leopardus lineages, indicating mtDNA does not suffer from incomplete lineage sorting for these species. In contrast, one of three nuclear markers (locus 7-90TG) differentiated the species into two reciprocally monophyletic clades, with no evidence of hybridisation or ancestral polymorphism. The remaining two nuclear markers (2-22 and ETS-2) did not separate these two species, while distinguishing other plectropomid species, suggesting incomplete lineage sorting at these nuclear loci. These results together with coalescence analyses suggest that P. leopardus females have hybridised historically with P. maculatus males and that P. maculatus mitochondria were displaced through introgressive hybridisation and fixation in the P. maculatus founder population on the Great Barrier Reef. The contrasting regional patterns of mtDNA structure may be attributed to Quaternary sea-level changes and shelf width differences driving different reef configurations on each coast. These reef configurations have provided opportunities for local scale interaction and reproduction among species on the narrower EA continental shelves, but not on the broader WA continental shelves.

Introduction

Coral reef fish faunas comprise high diversity assemblages that include closely related, co-occurring species of relatively recent origin (Clements et al., 2003, McMillan and Palumbi, 1997). Important features of present day fish faunas include abundant populations characterized by mixed-species spawning assemblages that are confined to shallow waters and have high reproductive outputs. Genealogical analysis of such populations has revealed evidence for hybridisation (e.g. van Herwerden and Doherty, 2006, Yaakub et al., 2006) or retained polymorphisms (e.g. Kai et al., 2002). This reflects the influence of both contemporary ecological events and historical episodes that have modified habitat structure and continuity and thus the associated populations over geological time. Given the restriction to shallow water habitats, reef fish populations provide an excellent opportunity to investigate how both contemporary ecological interactions and historical changes mediated by habitat disturbance have modified the genetic structures of populations of tropical marine vertebrates.

This study examines the genetic structure of two species of tropical groupers of the genus Plectropomus, P. leopardus (Lacapède 1802) and P. maculatus (Bloch, 1790). The genus comprises seven species, all associated with Indo-Pacific coral reefs. P. leopardus and P. maculatus, are the most abundant species, and are more widely distributed and abundant on the east coast of Australia relative to the west coast (personal communication, Choat), On each coast the species are partitioned by habitat, with P. leopardus characteristic of clearer water of midshelf and offshore reefs and P. maculatus more common on coastal reefs (Heemstra and Randall, 1993, Russ et al., 1996).

On the EA coast, the Great Barrier Reef (GBR) with parallel coastal, midshelf and off-shore reef systems extends continuously along a 1200 km latitudinal gradient (Fig. 1A). In contrast, WA coral reefs are patchy in their distribution. Coastal reef areas are widely separated by non-reef habitats, while offshore reefs comprising isolated islands and atolls occur over the same latitudinal gradient as the coastal reefs, but are widely separated from each other and from coastal habitats (Fig. 1B). Due to the narrow continental shelf of northeastern Australia midshelf reefs, the primary habitat of P. leopardus, these are adjacent to coastal reefs with the result that P. leopardus and P. maculatus frequently co-occur on that coast.

In contrast, the configuration of the WA reef systems means that the two species have non-overlapping local distribution patterns (Ayling and Ayling, 1987, Done et al., 1994, Hutchings, 1994). Despite the presence of P. maculatus in coastal waters of the Dampier Archipelago (A. Halford pers comm.), no individuals have been recorded from any of the off-shore sites (Done et al., 1994, Nardi et al., 2004). Moreover, the latitudinal distribution of both species on the west coast is patchy. For example, Ayling and Ayling (1987) recorded only four P. leopardus and no P. maculatus at the Ningaloo reef system.

van Herwerden et al. (2002) demonstrated that Australian east coast P. leopardus and P. maculatus could not be distinguished by a mitochondrial marker (HVR I), although minimal separation was achieved using a single nuclear marker (an oncogene intron, ETS2). These results with a matrilineal marker suggested that female P. leopardus had hybridised with male P. maculatus and that P. maculatus mitochondria have been displaced due to introgressive hybridisation. There were however three limitations to this study. First, the patterns observed were not adequately corroborated by the analysis of other nuclear genes, so incomplete lineage sorting, rather than hybridisation may be responsible for the observed lack of mtDNA differentiation between the two species. Secondly, sampling within and among habitats and regions was minimal with only five samples per species screened. Thirdly, no attempt was made to compare populations from localities other than the GBR where the species are spatially partitioned.

The present study is designed to further investigate our initial observation that introgressive hybridisation has occurred between P. leopardus and P. maculatus. Our primary hypothesis is that introgressive hybridisation has occurred on the EA coast due to the degree of ecological sympatry and overlap of reproductive sites of these two closely related species. Our prediction is that WA coast populations that are ecologically allopatric and have no access to common reproductive sites will have distinct mitochondrial lineages, unless incomplete lineage sorting and ancestral polymorphisms rather than introgressive hybridisation are responsible for the lack of mtDNA partitioning observed on the GBR. Such ancestral polymorphisms should affect populations from both regions, irrespective of their spatial partitioning whereas introgressive hybridisation should be apparent along the east, but not the west coast. Therefore, this study is designed to differentiate between the alternate hypotheses of mtDNA introgression and ancestral polymorphism.

The history of coral reef fish populations is closely linked to the history of their primary habitats. Sea level changes associated with glacial cycles have profoundly modified shallow water systems and thus the distribution patterns and genetic structures of their fish populations (Grant and Bowen, 1998). Well-documented time courses of sea level changes on both coasts of Australia coupled with tectonic stability (Nakada and Lambeck, 1989, Stirling et al., 1998) has allowed analysis of the probable history of Australian reef environments over the last one million years. This includes the closure of the Torres Strait from 116 to 30 kya (Hopley, 1982, Woodroffe et al., 2000) and the recent emergence of the modern Great Barrier Reef during the past 8–9 kya (Larcombe, 2004). The consensus of these geological studies suggests differing histories of sea-level change and reef formation in each region with EA coast reefs having a more recent history of disturbance than those of the WA coast (Lambeck and Nakada, 1990). Our secondary hypothesis is that the different histories of each region results in a coast-specific pattern of introgressive hybridisation. Habitat reductions during low sea level stands would result in population bottlenecks followed by different patterns of population expansion on each coast. East coast populations of P. leopardus and P. maculatus have been subject to more recent episodes of population contraction and expansion than west coast populations.

Our study required a comprehensive sampling program to obtain tissue samples from both species from each coastal region for which we have inferred differing reef histories. To evaluate the evidence for introgressive hybridisation or incomplete lineage sorting we employed both mitochondrial and nuclear markers.

Section snippets

Sampling procedures

On the east coast, samples were taken during the spawning season at latitudinal extremes of the reef system, extending from 10–23 °S, at sites where the two species occur sympatrically and at an intermediate, central location, where coastal and midshelf populations of the two species were sampled. Northern and central GBR sites and Hervey Bay were sampled by line fishing (as part of the CRC Torres Strait or Effects of Line Fishing Projects, Reef CRC), or by spearing from southern GBR sites. On

Phylogenetic analyses

The Akaike Information Criterion (AIC) approach, implemented in Modeltest version 3.06 (Posada and Crandall, 1998), identified the most appropriate substitution models for the given data to be the HKY + G with a gamma distribution shape parameter, G, of 1.133 to model rate variation across sites for HVR I sequences. Six substitution types (“nst = 6”), with base frequencies estimated from the data, were also specified for HVR I sequences. The nuclear locus 7-90TG required the JC substitution model

Introgressive hybridisation

The analysis of mitochondrial and nuclear markers from both species and both coastal regions yielded contrasting results. WA P. leopardus and P. maculatus mitochondria were genetically discrete, forming two reciprocally monophyletic clades. In contrast, there was a single mtDNA lineage regardless of species identity on the EA coast. This single lineage was sister to the WA P. leopardus lineage. The argument for inter-species mtDNA introgression is supported, not only by the observed contrasting

Conclusion

Analysis of a mitochondrial and a nuclear marker retrieved well-supported species phylogenies, with one exception. Australian east coast P. leopardus and P. maculatus were contained within a single mitochondrial clade. We conclude that this is the result of introgressive hybridisation, with or without a selective sweep and that this hybridisation is relatively ancient, despite the possibility of contemporary hybridisation. Analysis of the matrilineal marker suggests that the biological basis of

Acknowledgments

This study was funded by grants to JHC, LVH and MVO from James Cook University’s Program Grant Scheme, from the CRC Reef, the Smithsonian/STRI collaborative research program, and ARC and JCU Fellowships to LVH. We thank the ELF program, Reef CRC, Torres Strait CRC and D. Robertson for east coast samples, D. Souter QFA provided sample material from the east coast through the commercial sector. We thank Amos Mapleston for providing samples from Hervey Bay and Kim Nardi and Chris Dibden for

References (55)

  • K.D. Clements et al.

    Rapid evolutionary divergences in reef fishes of the family Acanthuridae (Perciformes; Teleostei)

    Mol. Phylogenet. Evol.

    (2003)
  • C.H. Stirling et al.

    Timing and duration of the last interglacial: evidence for a restricted interval of widespread coral reef growth

    Earth Planet Sci. Lett.

    (1998)
  • C.D. Woodroffe et al.

    Holocene reef growth in Torres strait

    Mar. Geol.

    (2000)
  • S. Adams et al.

    Geographic variation in the sex ratio, sex-specific size, and age structure of Plectropomus leopardus (Serranidae) between reefs open and closed to fishing on the Great Barrier Reef

    Can. J. Fish. Aquat. Sci.

    (2000)
  • B.J.R. Alvarado et al.

    Mitochondrial DNA control region sequences indicate extensive mixing of swordfish (Xiphias gladius) populations in the Atlantic Ocean

    Can. J. Fish. Aquat. Sci.

    (1995)
  • Anon

    ‘Sequencher’ Gene Codes Corporation

    (2000)
  • Ayling, A.M., Ayling, A.L. 1987. Ningaloo marine park:preliminary fish density assessment and habitat survey....
  • L.K. Bay et al.

    High genetic diversities and complex genetic structure in an Indo-Pacific tropical reef fish (Chlorurus sordidus): evidence of an unstable evolutionary past?

    Mar. Biol.

    (2004)
  • Buckworth, R.C., Newman, S.J., Ovenden, J.R., Lester, R.J.G., McPherson, G.R. 2006. The stock structure of northern and...
  • E.L. Cabot

    Eyeball sequence editor v3.1s

    (1997)
  • P.U. Clark et al.

    Rapid rise of sea-level 19,000 years ago and its global implications

    Science

    (2004)
  • T.J. Done et al.

    Surveys of coral and fish communities at Scott Reefs and Rowley Shoals. Produced in accordance with the Scott Reef research services agreement between Woodside Offshore Petroleum Pty. Ltd and the Australian Institute of Marine Science

    AIMS

    (1994)
  • N.G. Elliot

    Allozyme and mitochondrial DNA analysis of the tropical saddle-tail sea perch, Lutjanus malabaricus (Schneider), from Australian waters

    Mar. Freshw. Res.

    (1996)
  • L. Excoffier et al.

    Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data

    Genetics

    (1992)
  • B.P. Ferreira et al.

    Age, growth and mortality of the inshore coral trout Plectropomus maculatus (Pisces:Serranidae) from the central Great Barrier Reef, Australia

    Aust. J. Mar. & Freshw. Res.

    (1992)
  • B.P. Ferreira et al.

    Age validation and estimation of growth rate of the coral trout Plectropomus leopardus (Lacepede 1802) from Lizard Island, northern Great Barrier Reef

    Fisheries Bull.

    (1994)
  • A. Frisch et al.

    Field and experimental studies of hybridisation between coral trouts, Plectropomus leopardus and Plectropomus maculatus (Serranidae), on the Great Barrier Reef, Australia

    J. Fish Biol.

    (2006)
  • W.S. Grant et al.

    Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation

    Heredity

    (1998)
  • T. Hanebuth et al.

    Rapid flooding of the sunda shelf: a late-glacial sea-level record

    Science

    (2000)
  • Heemstra, P.C., Randall, J.E. 1993. Groupers of the world (Family Serranidae, subfamily Epinephelinae). An annotated...
  • Heyward, A.J., Pinceratto, E.J., Smith, L.D. 1997. Big bank shoals of the Timor Sea. An environmental resource atlas....
  • D. Hopley

    The geomorphology of the Great Barrier Reef: Quaternary development of coral reefs

    (1982)
  • J.P. Huelsenbeck et al.

    MRBAYES: bayesian inference of phylogenetic trees

    Bioinformatics Applications Note

    (2001)
  • Hutchings, B. 1994. A survey of the nearshore reef fish fauna of Western Australia’s west and south coasts-the Leeuwin...
  • Y. Kai et al.

    Genetic differences among three colour morphotypes of the black rockfish Sebastes inermis inferred from mtDNA and AFLP analyses

    Mol. Ecol.

    (2002)
  • T.D. Kocher et al.

    Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers

    Proc. Natl. Acad. Sci. USA

    (1989)
  • K. Lambeck et al.

    Late Pleistocene and Holocene sea-level change along the Australian Coast

    Paleogeo. Paleocli. & Paleoecol.

    (1990)
  • Cited by (0)

    View full text