Host-Associated Speciation in a Coral-Inhabiting Barnacle

O. Mokady and I. Brickner

The Institute for Nature Conservation Research
The Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel


    Abstract
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 Supplementary Material
 Acknowledgements
 literature cited
 
Host specificity of symbionts is considered an important factor associated with sympatric speciation. Here, we examine host specificity and the degree of host-associated speciation in the barnacle Savignium milleporum, an obligate symbiont of the hydrocoral Millepora (the "fire coral"). Little morphological variability was revealed between barnacles collected from two morphs of the hydrocoral Millepora dichotoma (encrusting or branching) or from its congener Millepora platyphylla, but a molecular analysis revealed an unexpected pattern of DNA sequence divergence. The sequences of the 12S mitochondrial rDNA were nearly identical within each of the three barnacle populations (average sequence divergence <1%), and the sequences obtained for barnacles collected from the two different morphs of M. dichotoma differed considerably (ca. 9% average sequence divergence). However, S. milleporum collected from M. platyphylla were nearly identical to the barnacles from the branching M. dichotoma (<0.5% average sequence divergence). The pattern of speciation demonstrated by Savignium barnacles indicates the gradual colonization of similar hosts (i.e., sequential evolution), rather then "casual" colonization, as indicated for other systems. If this is indeed so, then symbiont phylogeny should roughly correlate with host phylogeny. Additionally, the data support the "rendezvous host" hypothesis, which invokes the opportunity of both sexes to meet as a major component for which selection favors the costly habit of host specificity.


    Introduction
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 Supplementary Material
 Acknowledgements
 literature cited
 
One of the processes that may lead to the formation of sibling species complexes involves adaptation to specific habitats (Knowlton 1993Citation ). A special case of habitat specificity is that of epibiontic organisms, which specialize in inhabiting live hosts. The common observation for many animals that preferential mating occurs among individuals utilizing the same host or habitat has motivated the development of habitat preference speciation models (Diehl and Bush 1989Citation ). Diehl and Bush (1989)Citation demonstrated that habitat/host preference may be a powerful factor which can promote sympatric speciation.

Host-associated speciation is expected to be especially effective for sessile organisms, and more so when mating is restricted to occur between closely spaced individuals. Under such conditions, the host specificity of motile life stages (e.g., larvae) will account for recruitment to the specific substrate, and spatially restricted mating will lead to effective reproductive isolation and subsequent speciation (Templeton 1989Citation ).

Epizoic barnacles are sessile, marine crustaceans and constitute a model system featuring the above conditions (Darwin 1854Citation ; Newman and Ross 1976Citation ; Foster 1987Citation ). Barnacles of the subfamily Pyrgomatinae are obligate symbionts of stony corals or hydrocorals (Hiro 1935Citation ). They reproduce by internal fertilization, thus limiting potential mates for a given barnacle to the immediate neighbors. Following a period of embryonic development, pelagic larvae are released into the water column. These larvae must recruit to suitable substrates in order to metamorphose and become adults. Host specificity in the larvae will thus lead to the establishment of a reproductive barrier between barnacles inhabiting different hosts.

In a recent investigation (Mokady et al. 1999Citation ), it was shown that Savignium barnacles demonstrate high levels of host specificity and exhibit relatively large genetic distances between populations inhabiting different coral species. Specifically, Savignium dentatum barnacles extracted from a variety of coral hosts, clustered according to their host species based on DNA sequence analysis. In contrast, Cantellius barnacles were shown to display very low genetic variability across a wide phylogenetic and morphological range of coral hosts. Thus, Savignium and Cantellius demonstrate opposite strategies for inhabiting a variety of hosts, namely, speciation versus phenotypic plasticity, respectively.

Savignium milleporum is the only pyrgomatine occurring on the hydrocoral Millepora, of which it is an obligate symbiont (Ross and Newman 1973Citation ). (In the phylogenetic reconstruction presented by Mokady et al. [1999]Citation , S. milleporum did not cluster together with the other Savignium barnacles examined. This finding agrees with the assignment of S. milleporum to a separate, new genus—Wanella—based on functional morphology [Anderson 1992, 1993Citation ]. The nomenclature of pyrgomatides is a subject of ongoing revision. Throughout the current report, we use the name S. milleporum). In an essay on host specificity of coral-inhabiting barnacles, Ogawa and Matsuzaki (1992)Citation reported S. milleporum as a single species inhabiting a variety of Millepora hydrocorals, which is in line with the current systematic knowledge (reviews by Ross and Newman 1973Citation ; Newman and Ross 1976Citation ; Holthuis 1982Citation ). The remarkable morphological variability of Millepora (e.g., De Weerdt 1981Citation ) suggested to us that S. milleporum may in fact constitute a complex of host-specific sibling species. On the other hand, much of the variability of Millepora has been attributed to environmentally induced ontogenetic changes (De Weerdt 1984Citation ; Vago et al. 1998Citation ), and therefore it was difficult to predict the degree of specificity that S. milleporum would display.

The present study compares S. milleporum barnacles inhabiting three types of substrates available in the Gulf of Elat, Red Sea—the hydrocoral Millepora platyphylla and two morphs (encrusting and branching) of its congener Millepora dichotoma. Morphological and molecular parameters are used to identify similarities and dissimilarities between the barnacles.


    Materials and Methods
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 Supplementary Material
 Acknowledgements
 literature cited
 
Morphology
Fragments of colonies of the hydrocoral M. dichotoma (both encrusting and branching morphs) inhabited by S. milleporum barnacles were collected at a depth of 3–6 m near the H. Steinitz Marine Biology Laboratory, Elat, Red Sea, Israel.

The length and width of the parietal margins of the base were measured for individual barnacles under a dissecting microscope with the aid of a scaled ocular. (These dimensions are identical to the width and length of the barnacle's shell [see Newman and Ross 1976Citation , fig. 10]). Newly settled "young of the year" were easy to detect, and such individuals were excluded from the allometric analysis (the ratio between width and length) that attempted to characterize adults in each population.

Fragments were sampled from about 30 colonies of each morph of M. dichotoma, yielding more than 200 S. milleporum barnacles of each population. Millepora platyphylla, an upright, massive congener of M. dichotoma, could not be sampled as described above for reasons of nature conservation because it is much less abundant. Thus, only a very small number of barnacles were obtained from this hydrocoral (14 S. milleporum barnacles from 2 M. platyphylla colonies).

Data were statistically analyzed according to Sokal and Rohlf (1995Citation ; p. 243 for LSD test, p. 495 for F-test for equality of slopes).

DNA Preparation and Polymerase Chain Reaction Amplification
Individual barnacles were homogenized in 250 µl of a lysis buffer containing 7 M urea, 0.3 M NaCl, 0.05 M Tris-HCl (pH = 8), 0.02 M EDTA, and 1% sarcosine. Following homogenization, an equal volume of phenol : chlorophorm (1:1) was added, and tubes were shaken vigorously and incubated for 15 min at room temperature. Following phase separation by centrifugation, DNA was ethanol-precipitated. The polymerase chain reaction (PCR) was employed to amplify a fragment of the 12S subunit of the mitochondrial rDNA using the primer set of Kocher et al. (1989)Citation as modified by Mokady et al. (1994)Citation : 5'-GAAACCAGGATTAGATACCC and 5'-TTTCCCGCGAGCGACGGGCG. Amplification was carried out using 1 U of Taq DNA polymerase (Promega) in the presence of 2.5 mM MgCl2 and 0.1 mM of each dNTP. The amplification consisted of initial denaturation at 94°C for 2 min, followed by 40 cycles of denaturation at 94°C for 0.5 min, annealing at 50°C for 1 min, and elongation at 72°C for 0.5 min. The cycles were followed by a final elongation step of 72°C for 5 min.

Sequence Analysis and Phylogenetic Reconstruction
Direct sequencing was performed by fluorescent chain termination on an ABI 377 automated sequencer. Sequences were aligned using CLUSTAL V software (Higgins, Bleasby, and Fuchs 1992Citation ), and the aligned sequences were analyzed using PAUP*, version 4.0d65 (Swofford 1999Citation ). Distance matrices were produced using the "standard distances–total character difference" option. Both maximum-parsimony and maximum-likelihood criteria were used for phylogenetic reconstruction, with the transition/transversion (Ti/Tv) ratio estimated from the actual data (0.93).

Single-Strand Conformation Polymorphism
Amplification products were screened by single-strand conformation polymorphism (SSCP), an electrophoretic method which provides for identifying DNA sequence variation at a given locus (Orita et al. 1989Citation ). SSCP distinguishes between equal-length DNA fragments differing in sequence based on their molecular conformation (Lessa and Applebaum 1993Citation ).

Samples for SSCP analysis consisted of 5 µl of diluted PCR product (1:10–1:50 dilution, typically 1:30) supplemented with 5 µl of loading buffer (98% formamide, 10 mM EDTA, 0.025% xylene cyanol, 0.025% bromo-phenol blue). Samples were run on horizontal polyacrylamide gels (CleanGel 48 10% or 15%; ETC, Germany) according to the manufacturer's instructions.


    Results
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 Supplementary Material
 Acknowledgements
 literature cited
 
Morphology
Barnacles collected from branching M. dichotoma were found to be significantly larger in length and width than those from the encrusting morph (table 1 ). Barnacles from M. platyphylla, in turn, were significantly larger then those collected in branching M. dichotoma (however, the small sample size of barnacles from M. platyphylla must be kept in mind when considering these data; table 1 ). However, the allometric relationships (width vs. length) commonly used to compare barnacles were very similar in all three populations (table 1 ).


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Table 1 A Comparison of Lengths and Widths of Burrow Openings Between Savignium milleporum Barnacles Collected from Encrusting (E) and Branching (B) Millepora dichotoma and Millepora platyphylla

 
Molecular Analysis
A ~400-bp fragment of the 12S mt rDNA was amplified from a total of 33 S. milleporum barnacles—15 and 14 from the populations inhabiting the branching and encrusting morph of M. dichotoma, respectively, and 4 from the population inhabiting M. platyphylla. Figure 1 compares the sequences obtained from two individual barnacles of each population, each sampled from a separate Millepora colony. Barnacles inhabiting the two morphs of M. dichotoma showed <1% sequence divergence within populations and >9% between populations. Interestingly, the sequence obtained for barnacles sampled from M. platyphylla was nearly identical to that obtained for individuals from branching M. dichotoma.



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Fig. 1.—Alignment of partial sequences of the 12S mt rDNA fragments amplified from Savignium milleporum barnacles (EMBL database accession numbers AJ277296–AJ277301). Barnacles are identified by the hosts from which they were collected—Millepora dichotoma B (branching), M. dichotoma E (encrusting), and Millepora platyphylla. Each sequence represents an individual barnacle collected from a separate colony. A dot in a sequence indicates that the nucleotide in that position is the same as that in the "M. dichotoma B 1" sequence at the top.

 
The pattern of differences shown in figure 1 was further confirmed by sequence analysis using additional barnacles from each of the populations inhabiting branching and encrusting M. dichotoma (six and five additional sequences, respectively; see Supplementary Material for accession numbers and file name). Table 2 shows average percentages of sequence divergence calculated for all possible pairwise comparisons and the range of percentage of sequence divergence observed for each class of between-populations comparisons.


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Table 2 Pairwise Sequence Divergence Observed in this Study

 
In addition to the 17 amplification products subjected to sequence analysis, 16 products were analyzed by SSCP—seven from each of the populations inhabiting branching and encrusting M. dichotoma and two from the population inhabiting M. platyphylla. Figure 2 shows the banding pattern obtained in one of the SSCP gels, in which 13 of the 16 samples were analyzed. Note the lanes in which the analyzed product was also sequenced, providing a "calibration" tool for the SSCP analysis. The data obtained through SSCP analysis fully supported the pattern emerging from the above sequence analysis. All barnacles collected from encrusting M. dichotoma displayed the same banding pattern, which was clearly different from that displayed by all barnacles collected from either branching M. dichotoma or M. platyphylla (however, only four barnacles were examined from the latter).



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Fig. 2.—Single-strand conformation polymorphism (SSCP) analysis of 12S mt rDNA fragments amplified from Savignium milleporum barnacles. Each lane represents an individual barnacle. The hosts are indicated at the top, and separate colonies of each host are indicated by roman numerals. One or two barnacles were sampled from each colony. Fragments in the lanes marked by asterisks are those aligned in figure 1

 
The sequences shown in figure 1 were used for a phylogenetic reconstruction, together with representative homologous sequences previously obtained for other barnacles (Mokady et al. 1999Citation ). The reconstructed tree is shown in figure 3 . Maximum-parsimony analysis yielded 18 equally parsimonious trees of 237 steps. Maximum-likelihood analysis produced a tree which was in agreement with that represented by a "majority-rule" consensus tree produced by maximum parsimony, with the exception of the relative positions of individual sequences within the two S. milleporum subclades.



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Fig. 3.—A reconstruction of the phylogenetic relationships between Savignium barnacles. The substrate from which each barnacle was collected, either a coral/hydrocoral host or dead rock, is specified in parentheses. The six sequences aligned in figure 1 were compared with sequences obtained in a previous study (Mokady et al. 1999Citation ; sequences marked with an asterisk). The topology of the tree and the branch lengths (see scale at the bottom) are those produced by maximum-likelihood analysis. A "50% majority rule" of 18 equally parsimonious trees supports the presented topology. Values to the left of a node relate to the maximum-parsimony analysis: the number of changes along a branch leading to the node is indicated, according to the parsimony-derived tree showing this precise topology, and the percentage of the 18 trees in which the group to the right of the node occurred is indicated in parentheses.

 

    Discussion
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 Supplementary Material
 Acknowledgements
 literature cited
 
The Barnacle Symbionts
Savignium barnacles have been reported in previous studies to be specific to coral suborders (Ross and Newman 1973Citation ) and genera (Ogawa and Matsuzaki 1992Citation ; Mokady et al. 1999Citation ). In the current study, S. milleporum is shown to be specific at a further level—host morph within host species. The maximum within-population pairwise sequence divergences observed were 1.6% (5 nt) and 1.1% (4 nt) for barnacles from encrusting and branching M. dichotoma, respectively. The two sequences obtained for barnacles inhabiting M. platyphylla were also nearly identical (table 2 ). In contrast, the average pairwise sequence divergence between barnacles from the encrusting M. dichotoma and either of the other populations examined was considerably larger (up to 10.35%, 38 nt).

The magnitude of the observed sequence divergence resembles that obtained for S. dentatum barnacles (Mokady et al. 1999Citation ). The average pairwise sequence divergences between individual S. dentatum collected from different coral species or from different colonies of the same coral species were 8.3% and 0.7%, respectively. However, the hosts of S. dentatum are corals belonging to different species and genera within a family (Faviidae), whereas the hosts examined in the current study represent two species within a genus and two morphs within a species. Therefore, the observed divergence of S. milleporum, probably indicating speciation, was achieved over a narrower taxonomic range of hosts. Unfortunately, knowledge regarding the phylogeny of the hosts is still lacking, and it is currently impossible to correlate phylogenetic distances between the hosts with observed sequence divergence (i.e., speciation) between their symbionts.

In contrast to different S. dentatum varieties (Mokady et al. 1999Citation ), where morphological differences between populations were evident, the current study did not reveal any clear morphological differences. However, only two dimensions of the barnacle's shell were measured, and considerable variability may exist in various "soft" body parts. The typical deposition of host skeletal material over the shell of S. milleporum (see Mokady et al. 1999Citation , fig. 3B ) did not allow examination of shell texture, which proved variable in S. dentatum. Further research may or may not identify morphological differences between the barnacle populations. It is nevertheless interesting to note here that morphological similarity may be caused by a range of evolutionary processes, including the following extremities. On one hand, rapid speciation may cause morphological changes to lag behind changes observed in highly variable DNA sequences. Conversely, the same pattern may reflect similar morphological selective pressures experienced on similar hosts.

The average sequence divergence between S. milleporum collected from branching M. dichotoma and those from M. platyphylla was <0.5%. This similarity is of special interest in light of the extreme differences between barnacles from encrusting M. dichotoma and those from the other hosts. We interpret the similarity between the barnacles to reflect some sort of similarity between their hosts—the branching morph of M. dichotoma and M. platyphylla. For example, the erect posture typical of these substrates, as opposed to the flat posture of the encrusting M. dichotoma, may promote settlement of barnacles with different swimming characteristics.

The Hydrocoral Hosts
The similarities and dissimilarities observed between the symbiotic barnacles prompt a discussion of their hosts, namely, Millepora hydrocorals. The different morphs of M. dichotoma were recently argued to be stages in an ontogenetic sequence (Vago et al. 1998Citation ). This suggestion is in line with the considerable morphological plasticity described for other Millepora species (De Weerdt 1981, 1984Citation ), including branching, encrusting, and robust morphs in any one of a variety of species. Of the four morphs examined by Vago et al. (1998)Citation , two are represented in this study by their S. milleporum inhabitants. Barnacles were sampled from different regions of the host, including the tips and base of the same branching colony. The near identity of DNA sequence within population and the substantial sequence divergence between populations inhabiting the different morphs do not provide support for the suggested ontogenetic course of the hydrocoral. This is especially emphasized by the identity revealed between barnacles collected in the course of this study from the flat, encrusting bases and from the branches of branching M. dichotoma colonies.

The Evolution of Host Specificity
Larvae of Savignium coral-inhabiting barnacles need to locate a specific host for recruitment (Hiro 1935, 1938Citation ; Mokady et al. 1999Citation ), which is a very costly habit. As these free-living stages have very limited capabilities of controlling their movements in the surrounding medium, most larvae are likely never to recruit. This resembles the situation for aphids (Homoptera: Aphididae), a model system in which the evolution of host specificity has been examined in depth. Dixon (1998)Citation reviews the research devoted to aphid host specificity and to presumably associated sympatric speciation. He discusses a number of hypotheses put forward to account for the evolution of host specificity in aphids, considering selection regimes, which may favor host specificity under the high costs associated with locating a specific host.

The "host utilization" hypothesis invokes a tradeoff between the high cost of locating a specific host and the reward of eventual settlement on a host which can be "best utilized" by the symbiont. Testing the applicability of this hypothesis for coral-inhabiting barnacles would require experimental settlement of different barnacles on different hosts and subsequent analysis of their performance (preferably in terms of lifetime reproductive output, which would require long-term experiments). Furthermore, the lack of parthenogenetic generations in barnacles diminishes the amplification of minute differences between hosts into substantial differences in fitness, as in aphids (Kindlmann and Dixon 1994Citation ). However, an examination of life history parameters in two barnacles sharing the same coral host supports another prediction of the host utilization hypothesis, namely, that specialists would outperform generalists on the same substrate. The specialist barnacle S. dentatum performs better then the generalist Cantellius pallidus when inhabiting their mutual host Cyphastrea chalcidicum (Brickner 1994Citation ). For example, in 15 of 17 C. chalcidicum colonies sampled, S. dentatum outnumbered C. pallidus, constituting 86% ± 15% of the total number of barnacles on the colony (80% ± 23% when all 17 colonies were included). Brickner (1994) gives a detailed comparison of the life history of these barnacles, including recruitment characteristics, reproductive parameters, longevity, and other parameters, indicating the relative success of S. dentatum.

The ‘rendezvous host’ hypothesis proposes that selection favors host specificity despite the great risks of dispersal because hosts serve not only as habitats and sources of nutrients, but mainly as rendezvous sites for the sexes (Ward et al. 1998Citation ). Dixon (1998)Citation points out that the importance of finding a mate on the host is most extreme in the aphids that lose their wing muscles following settlement and can no longer migrate. Like many other barnacles, coral-inhabiting barnacles feature a number of key characteristics which lend support to the applicability of the rendezvous host hypothesis (Ward 1991Citation ) to their case: (1) a completely sessile mode of life, being embedded in the host's skeleton for the duration of their adult life; (2) lack of asexual reproduction or self-fertilization; (3) internal fertilization, which requires close proximity to potential mates; and (4) clumped distribution, which answers the need for proximity (recorded, for example, for Savignium barnacles; unpublished data).

Since live substrates feature a biological component in addition to the structure and texture typifying any substrate (including dead substrates), live-substrate-inhabiting barnacles have more to gain by specializing on specific hosts. The lack of specificity in rock-inhabiting, intertidal barnacles (commonly observed on docks and other nearshore structures) may also be related to the predictability of substrate location. The shore is continuously lined with potential dead substrates, and there is no need for the larvae to perform "macrolocation" (they do need to perform "microlocation," having arrived at an intertidal rock, to assure proximity to potential mates). In contrast, live hosts are not guaranteed to be at all locations, and macrolocation must also be performed. The "cost" of host location is accordingly higher (e.g., energy expenditure, presettlement mortality), and the increased chance of finding a mate is hypothesized to compensate for increased cost.


    Conclusions
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 Supplementary Material
 Acknowledgements
 literature cited
 
It is clearly desirable to complement the existing knowledge regarding Savignium and other coral-inhabiting barnacles (e.g., Cantellius) with experimental assessment of settlement preferences, similar to studies carried out for the coral-inhabiting bivalve Lithophaga (Mokady et al. 1991, 1992Citation ). Further molecular information should also be obtained to verify the results obtained for the mitochondrial gene examined here, including data on nuclear genes, the divergence of which should also reflect the reproductive barriers assumed to exist. These barnacles will then offer a comparative database for testing hypotheses formulated for other model systems regarding speciation. Additionally, efforts should be devoted to studying the phylogenetic relationships between the hosts. This will enable us to estimate whether there has been sequential evolution of host and symbiont or, as in aphids, "a casual acquisition of ... new or ‘wrong’ hosts" (H. L. G. Stroyan in the discussion that follows Eastop 1973Citation ). The fact that both S. dentatum and S. milleporum show speciation within a narrow taxonomic range of available hosts in the Red Sea (a single family and a single genus, respectively) indicates the former possibility.


    Supplementary Material
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 Supplementary Material
 Acknowledgements
 literature cited
 
Seventeen newly reported sequences resulting from this study were deposited in the EMBL database under accession numbers AJ277296–AJ277301 and AJ295952–AJ295962. A ClustalV-generated alignment of these sequences was deposited under accession number ds44436.


    Acknowledgements
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 Supplementary Material
 Acknowledgements
 literature cited
 
We are grateful to the Tobias Landau Foundation for generous support of this research, and to Ms. L. Levi for technical assistance. Thanks are also due to the H. Steinitz Marine Biology Laboratory, at the Interuniversity Institute of Elat for the use of diving facilities and the hospitality of its staff. We thank M. Inbar for insightful comments.


    Footnotes
 
Dan Graur, Reviewing Editor

1 Keywords: cirripedia host specificity hydrocoral Millepora Savignium milleporum speciation Back

2 Address for correspondence and reprints: O. Mokady, Institute for Nature Conservation Research, Tel Aviv University, Tel Aviv 69978, Israel. mokady{at}post.tau.ac.il . Back


    literature cited
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 Supplementary Material
 Acknowledgements
 literature cited
 

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Accepted for publication January 31, 2001.





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Articles by Mokady, O.
Articles by Brickner, I.