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Observation Article
Revised

A pre-zygotic barrier to hybridization in two con-generic species of scleractinian corals

[version 2; peer review: 2 approved]
PUBLISHED 01 Nov 2013
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Abstract

Hybridization is often cited as a potential source of evolutionary novelty in the order Scleractinia. While hybrid embryos can be produced in vitro, it has been difficult to identify adult hybrids in the wild. Here, we tested the potential for hybridization between two closely related species in the family Fungiidae. We mixed approximately 5000 eggs of Ctenactis echinata with sperm from C. crassa. No hybrid embryos were produced. This observation adds to a growing body of evidence for pre-zygotic barriers to hybridization in corals and challenges the claim that hybridization is a major source of evolutionary novelty in the order.

Revised Amendments from Version 1

In response to feedback from the reviewers, we have updated our Observation Article as follows. In response to comments by Yossi Loya, we now note in the text that we did not quantifiy the viability of the Ctenactis echinata eggs by crossing them with C. echinata sperm because no sperm was available at the time. We have also corrected one citation. In response to a comment by Bernie Degnan, suggesting we had only looked at 100s of eggs, we now state that none of the approximately 5000 C. echinata eggs exposed to C. crassa sperm were fertilized. In response to email correspondence with Dr Bert Hoeksema, we have changed the name of the species in Figure 1 C & D from Fungia repanda to F. fungites. We have also provided more detail on how the Ctenactis species were identified and have corrected the relevant citation.

See the authors' detailed response to the review by Bernie Degnan
See the authors' detailed response to the review by Yossi Loya

Observation

Hybridization is a controversial topic in coral reef ecology1,2. While small numbers of hybrid embryos can be produced in a few species in vitro3, the evidence for hybrids in the field is often equivocal because the genetic techniques used for corals cannot distinguish between hybridization and incomplete lineage sorting4. In fact, only one of the over 1300 species in the order is generally accepted to be unequivocally of hybrid origin: Acropora prolifera1,5. Nonetheless, hybridization is often invoked as a source of evolutionary novelty in the order Scleractinia6,7.

Here, we report an incidental observation on the potential for hybridization between two closely related scleractinian corals species in the family Fungiidae, Ctenactis echinata and C. crassa. These species are sympatric, often dominating large multi-specific assemblages of fungiid corals throughout the central Indo-Pacific8. These species can generally be distinguished on the basis of the density of septa and the shape of septal dentitions, however, in Okinawa, these features are very similar and the most useful diagnostic character is a strong arch in the corallum of C. crassa (Figure 1A and B)9. Both species are gonochoric, that is each colony is either male or female, and reproduce by broadcast spawning, releasing gametes into the water column for fertilization8 (Figure 1C and D). At our study site on Sesoko Island (26°38'13.00"N; 127°51'56.24"E), Okinawa, Japan, spawning occurs following the full moons from July to August8. Furthermore, both species release gametes at the same time8 and consequently there is the potential for hybridization. In the days before the predicted date of spawning in July 2013, we collected four colonies of C. echinata and six colonies of C. crassa, to produce larvae for other experiments.

b11d6f13-1afa-4009-83bc-12abafcc832c_figure1.gif

Figure 1. Study species and broadcast spawning in fungiid corals.

Live Ctenactis echinata (A) and C. crassa (B) in aquaria prior to being isolated for spawning. Each colony is approximately 20 cm in length. Coral species in the family Fungiidae, such as these colonies of Fungia fungites, are gonochoric broadcast spawners: each individual releases either eggs (C) or sperm (D) into the water column where fertilization takes place (arrows indicate gametes).

While the species are relatively easy to identify, determining the sex of each individual prior to spawning is impossible without destructive sampling to expose the gametes. Consequently, we placed each individual in a separate 20 L bucket containing sea water in the open air at approximately 20:00 h in order to sex each individual once gametes had been released. On the night of 27 July between 22:30 and 23:30 h three C. echinata and five C. crassa spawned revealing that the three spawning C. echinata were female, while four C. crassa were females and one was a male. The size of the eggs of each species at the time of release was distinct with a range in maximum diameter of 244–266 μm in C. echinata and 133–155 μm in C. crassa. In contrast to earlier work on C. echinata10, we saw no symbiotic algae in the eggs of either species. We collected approximately 5000 eggs from the three C. echinata females and mixed them with sperm from the C. crassa male. The viability of the C. crassa sperm was tested by mixing it with C. crassa eggs, however, we could not quantify the viability of the C. echinata eggs because no C. echinata sperm was available on the evening of the experiment. Nonetheless, eggs from these colonies of C. echinata did produce viable larvae for use in later experiments. Approximately 100 eggs were observed under a stereo-dissecting microscope for cleavage, indicating fertilization, every 2 to 6 h over the next 24 h. At no point did we observe cleavage in the cross between species indicating that no hybrid embryos were produced and none of the approximately 5000 eggs remained intact after 24 h. In contrast, over 90% of C. crassa eggs in the positive control were fertilized within 2 h. We conclude that despite synchrony in the time of gamete release between these two closely related sympatric species there appears to be strong pre-zygotic mechanism to avoid hybridization. While our observations are preliminary and in only one direction (i.e. we did not cross C. echinata males with C. crassa females) we predict that hybridization between these species is unlikely. This observation adds to a growing body of evidence indicating strong pre-zygotic barriers to hybridization in many scleractinian corals1113.

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VERSION 2 PUBLISHED 20 Sep 2013
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Baird AH, Cumbo VR, Figueiredo J and Harii S. A pre-zygotic barrier to hybridization in two con-generic species of scleractinian corals [version 2; peer review: 2 approved]. F1000Research 2013, 2:193 (https://doi.org/10.12688/f1000research.2-193.v2)
NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article.
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Current Reviewer Status: ?
Key to Reviewer Statuses VIEW
ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions
Version 2
VERSION 2
PUBLISHED 01 Nov 2013
Revised
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14
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Reviewer Report 23 Jan 2014
Bernie Degnan, School of Biological Sciences, University of Queensland, Brisbane, Australia 
Approved
VIEWS 14
I confirm that I have read this submission and believe that I have an ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Degnan B. Reviewer Report For: A pre-zygotic barrier to hybridization in two con-generic species of scleractinian corals [version 2; peer review: 2 approved]. F1000Research 2013, 2:193 (https://doi.org/10.5256/f1000research.2862.r3281)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
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14
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Reviewer Report 13 Nov 2013
Yossi Loya, Department of Zoology, Tel Aviv University, Tel Aviv, Israel 
Approved
VIEWS 14
I note that the authors preferred to retain Figures 1C and 1D in spite of my recommendation to delete them, since they have nothing to do with the contents of the article. I do not insist that they do it, ... Continue reading
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CITE
HOW TO CITE THIS REPORT
Loya Y. Reviewer Report For: A pre-zygotic barrier to hybridization in two con-generic species of scleractinian corals [version 2; peer review: 2 approved]. F1000Research 2013, 2:193 (https://doi.org/10.5256/f1000research.2862.r2372)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
Version 1
VERSION 1
PUBLISHED 20 Sep 2013
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19
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Reviewer Report 24 Oct 2013
Bernie Degnan, School of Biological Sciences, University of Queensland, Brisbane, Australia 
Approved
VIEWS 19
This Observation Article reports the lack of cross-fertilization between Ctenactis echinata and Ctenactis crassa, closely related fungiid corals that naturally release gametes at the same time. The authors recognise the limitations of this observation - only small numbers of eggs (100's) ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Degnan B. Reviewer Report For: A pre-zygotic barrier to hybridization in two con-generic species of scleractinian corals [version 2; peer review: 2 approved]. F1000Research 2013, 2:193 (https://doi.org/10.5256/f1000research.2411.r1878)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response (F1000Research Advisory Board Member) 26 Oct 2013
    Andrew Baird, Australian Research Council, Centre of Excellence for Coral Reefs Studies, James Cook University, Townsville, Australia
    26 Oct 2013
    Author Response F1000Research Advisory Board Member
    Dear Bernie,

    Thank you for your comments. We would just like to point out that while we only examined 100 eggs every few hours under the microscope, we used approximately 5000 ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response (F1000Research Advisory Board Member) 26 Oct 2013
    Andrew Baird, Australian Research Council, Centre of Excellence for Coral Reefs Studies, James Cook University, Townsville, Australia
    26 Oct 2013
    Author Response F1000Research Advisory Board Member
    Dear Bernie,

    Thank you for your comments. We would just like to point out that while we only examined 100 eggs every few hours under the microscope, we used approximately 5000 ... Continue reading
Views
14
Cite
Reviewer Report 22 Oct 2013
Yossi Loya, Department of Zoology, Tel Aviv University, Tel Aviv, Israel 
Approved
VIEWS 14
  • The title is appropriate for the content of the article. The abstract represents a suitable summary of the work. Please correct: crass to crassa, in the 3rd line of the Abstract.
     
  • Article content: The design, methods and analysis of the results been clearly explained
... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Loya Y. Reviewer Report For: A pre-zygotic barrier to hybridization in two con-generic species of scleractinian corals [version 2; peer review: 2 approved]. F1000Research 2013, 2:193 (https://doi.org/10.5256/f1000research.2411.r2160)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response (F1000Research Advisory Board Member) 26 Oct 2013
    Andrew Baird, Australian Research Council, Centre of Excellence for Coral Reefs Studies, James Cook University, Townsville, Australia
    26 Oct 2013
    Author Response F1000Research Advisory Board Member
    Dear Yossi,

    Thank you for your comments. We have corrected the typos you identified, changed the reference as requested and added a sentence to clarify the controls that were used to ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response (F1000Research Advisory Board Member) 26 Oct 2013
    Andrew Baird, Australian Research Council, Centre of Excellence for Coral Reefs Studies, James Cook University, Townsville, Australia
    26 Oct 2013
    Author Response F1000Research Advisory Board Member
    Dear Yossi,

    Thank you for your comments. We have corrected the typos you identified, changed the reference as requested and added a sentence to clarify the controls that were used to ... Continue reading

Comments on this article Comments (0)

Version 2
VERSION 2 PUBLISHED 20 Sep 2013
Comment
Alongside their report, reviewers assign a status to the article:
Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
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