Molecular phylogeny of large miliolid foraminifera - University of ...

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70M. Holzmann et al. / Marine Micropaleontology 43 2001) 57±741977) who considered Parasorites and Broeckina astwo phylogenetically and geographically distinctgenera. Our observations con®rm that the testsof Caribbean Broeckina are delicate and morefragile than those of Paci®c Parasorites, asmentioned by Levy 1977). Further externalmorphological differences between these twogenera concern the arrangement and appearanceof marginal apertures. In Parasorites, themarginalapertures are oval-shaped and arranged perpendicularto the apertural face Plate 2, Fig. 2),whereas the marginal apertures of Broeckina areelongated and surrounded by a calci®ed rim. Theyare arranged parallel to the apertural face Plate 3,7). Moreover, some ecological differences existbetween the two taxa: while living specimens ofBroeckina are typically found on reef rubble in15±30 m depth Hallock and Peebles, 1993),Parasorites prefers sandy substrates and can befound up to 80 m depth Hohenegger et al., 1999).The taxonomic status of both genera needs to berevised. Broeckina was classi®ed in the Soritinae byMunier-Chalmas 1882) and in the family Meandropsinidaeby Levy 1977) and Crapon de Capronad'Ersu 1985), but our genetical analyses clearly indicatethat Broeckina is a member of the Archaiasinae.The phylogenetic position of Parasorites as inferredfrom molecular data suggests a basal relation withSoritinae Figs. 1 and 2). This would be in agreementwith Hofker 1953) who put Praesorites orbitolitoidesat the base of the Soritinae. Hofker 1953) assumesthat P. orbitolitoides developed from archaiasineancestors, but its internal skeleton shows typical soritinecharcteristics Hofker, 1952). Molecular relationshipsbetween Parasorites and the Soritinae, however,are supported by relatively low bootstrap values 60±70%) and phylogenetic analysis of all chlorophyteendosymbionts from Archaiasinae and Parasoritesreveals a single origin for the green algae Pawlowskiet al., 2001a,b). The taxonomic position of Parasoritesstays thus a point of discussion.4.4. Soritinae consist of two sister clades: Sorites/Marginopora vertebralis and Sorites/Amphisorus/M.cf. kudakajimaensisMolecular data shed new light on the phylogeny ofSoritinae. The general view of evolution within thisgroup goes from simple forms Sorites) to morecomplex Amphisorus) to highly differentiated onesMarginopora) Lehmann, 1961). The increase ofmorphological complexity is illustrated by the developmentof a duplex skeleton Amphisorus), doublingof annular canals and appearance of auxilliary chamberletsMarginopora) Lehmann, 1961; Gudmundsson,1994). According to our results Figs. 1±4), thegenus Amphisorus is a sister group to Sorites and doesnot branch between Sorites and Marginopora, aswould be expected if the evolution of Soritacea wasdriven by progressive morphological complexity.Moreover, it seems that the evolution of highly differentiatedforms has taken place independently at leasttwice: Marginopora vertebralis and another form thatwas identi®ed as Marginopora cf. kudakajimaensis,cluster separately, the ®rst one as the sister group tothe genus Sorites, the second one branches within thegenus Amphisorus Fig. 4).Our results are supported by morphological studies.A comparison of three specimens of Marginoporavertebralis d, e, f) and two specimens of Marginoporacf. kudakajimaensis b, c), where half of the testwas used for DNA extraction and the other half wasinvestigated with the SEM, revealed that both speciesshow some similarities with Sorites and Amphisorus,respectively Plate 1, 1±4; Plate 2, 1±6). The aperturesin M. vertebralis are rounded to circular with acalci®ed rim like in Sorites, while the apertures in M.cf. kudakajimaensis have an elongated to irregularshape as in Amphisorus. The chamber sutures inSorites and M. vertebralis are wave-like, whereasthey are slightly rounded in Amphisorus and in someM. cf. kudakajimaensis specimens. The investigatedspecimens of M. cf. kudakajimaensis show an internalmedian skeleton as it was described for M. kudakajimaensisGudmundsson, 1994). The internal skeleton,however, is only poorly developed in our forms.Because of their small size, it is dif®cult to decidewhether our investigated specimens represent juvenileforms of M. kudakajimaensis or belong to a new, yetunknown species. Further molecular and morphologicalstudies are necessary to clarify this question. Ataxonomic revision, however, should be undertakenfor the genus Marginopora as M. vertebralis clusterswithin another soritid genus.More detailed morphological studies are needed toexplain the presence of two genetically distinct groups
M. Holzmann et al. / Marine Micropaleontology 43 2001) 57±74 71within the genus Amphisorus Fig. 4). One groupcontains two soritid specimens that resemble insome external aspects Amphisorus, while the othercomprises several specimens of Amphisorus hemprichiiand Marginopora cf. kudakajimaensis. Morphologicalexamination of the ®rst group showed thatSorites sp._k and Sorites sp._l have thin tests and adelicate appearance, with a test diameter not exceeding3 mm. A test fragment from Sorites sp._l wasinvestigated with the SEM Plate 1, 5 and 6). Thespecimen has elongated to irregular shaped aperturesand slightly rounded chamber sutures, comparableto Amphisorus Plate 1, 3 and 4). Similar specimenswere described as Sorites orbiculus var.marginalis by Gudmundsson, 1994. From a molecularpoint of view, Sorites sp._k and Sorites sp._lmay represent a different, ancestral lineage fromwhich most of the recent Amphisorus species haveevolved.Morphological revision is needed in the case ofSorites, as it seems to be a paraphyletic group.Furthermore, two extant species of this genus, Soritesorbiculus and Sorites marginalis are not geneticallyseparated and seem to be morphological variants ofone species, an idea that was already proposed byGudmundsson 1994). On the other hand, a Soritesspecimen from Guam S. orbiculus_h) branches atthe basis of the whole Sorites/Marginopora cladeFig. 4), indicating that morphologically similarforms of S. orbiculus might be divided in differentgenotypes. Interestingly, two specimens of Soritescollected in Caribbean Sea, S. orbiculus_c and S.marginalis_d mingle with Indo-Paci®c representativesof this genus. This suggests that migration oflarge foraminifera between these two regions is possible,and more than a geographic barrier is needed toexplain the isolation of Caribbean Archaiasinae.4.5. Evolution of Soritacea is driven by endosymbiosisOur data indicate that the acquisition and change inalgal types as endosymbionts were crucial steps in theevolution of large miliolid foraminifera. The moleculardivision of Soritacea in three groups largely correspondsto their division based on different algalendosymbionts as proposed by Lee and Anderson1991). The unique character of each symbiont transformationis con®rmed by our molecular phylogeneticstudies of soritid symbionts. Phylogenetic analysis ofsymbiont rDNA sequences reveals a single origin ofall chlorophyte-symbionts found in Archaiasinae,including Parasorites Pawlowski et al., 2001a,b). Asimilar study shows that the majority of Symbiodinium-likesymbiotic dino¯agellates in Soritinae arespeci®c to foraminiferans and do not mix withSymbiodinium-like symbionts of corals and othermarine invertebrates Pawlowski et al., 2001a,b).Very little is known about the mechanisms ofsymbiont acquisition by foraminiferans. Our resultsindicate, that two factors play a certain role in theprocessus of divergence and radiation of a newgroup of symbiont-bearing foraminiferans. The ®rstone is the necessity of morphological adaptation to aparticular type of symbionts. For example, allmembers of the Soritinae are distinguished bydiscoidal tests with septula as internal partitionsLehmann, 1961). Their ¯at tests with a largesurface/volume area are optimized for sunlightcapture and appear to be ef®cient in the uptake ofnutrients that are diffusing from the underlyingsubstratum Hallock et al., 1991; Hallock and Peebles,1993). Discoidal tests also evolved several times inArchaiasinae, but with a different internal skeletonSeiglie et al., 1976; Gudmundsson, 1994). If soritineforaminiferans originate from Archaiasinae Hofker,1953; Haynes, 1981), then discoidal tests might havebeen passed on by the last common ancestor of Soritinaewhich could have had morphological characterssimilar to that of Parasorites Hofker, 1953).The radiation of larger foraminiferan lineagesappears to be related to the ecological requirementsof their symbionts Hallock, 1999). Chlorophyceansymbionts are known to be less effective in providingtheir hosts with nutrients than dino¯agellates Hallockand Peebles, 1993). It is therefore not surprising thatdino¯agellate-bearing Soritinae are abundant anddiverse on oligotrophic Indo-Paci®c coral reefs, butare not as common in the more mesotrophic waters ofwestern Atlantic. Inversely, chlorophyte-bearingArchaiasinae radiated in the Caribbean Sea, whilerecent representatives of this group are uncommonin the Indo-Paci®c Debenay, 1985; Haig, 1988;Hallock and Peebles, 1993; Hohenegger, 1994; Hoheneggeret al., 1999). As proposed by Hallock 1988a,b),the biogeographic patterns of distribution of the Soritaceaappear to be related to the evolutionary history of
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