Peristome Development in Mosses in Relation to Systematics and Evolution. II. Tetraphis pellucida (Tetraphidaceae) Author(s): Jonathan Shaw and Lewis E. Anderson Source: American Journal of Botany, Vol. 75, No. 7 (Jul., 1988), pp. 1019-1032 Published by: Botanical Society of America Stable URL: http://www.jstor.org/stable/2443770 Accessed: 11/11/2010 06:37 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=botsam. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Botanical Society of America is collaborating with JSTOR to digitize, preserve and extend access to American Journal of Botany. http://www.jstor.org Amer. J. Bot. 75(7): 1019-1032. 1988. PERISTOME DEVELOPMENT IN MOSSES IN RELATION TO SYSTEMATICS AND EVOLUTION. II. TETRAPHIS PELLUCIDA (TETRAPHIDACEAE)1 JONATHAN SHAW2 AND LEWIS E. ANDERSON Departmentof Botany, Duke University, Durham, North Carolina27706 ABSTRACT The Tetraphidaeis a small subclass of mosses with a nematodontous peristome that has frequentlybeen interpretedas primitiveamong the truemosses. The developmentalcell sequence leading to the formationof the four peristometeeth of Tetraphispellucida is describedfor the firsttime. Comparisonsare made with sequencesknown for other nematodontousand arthro- dontous mosses. Peristomedevelopment in T. pellucidais more like that describedpreviously for arthrodontousperistomes than to published developmentalsequences for nematodontous peristomesof species in the Polytrichaceae.On the other hand, our observationsconfirm a basic uniformityof the earliestdevelopmental stages in all mosses studiedthus far, regardlessof their systematicposition. THE TETRAPHIDAEis the smallest subclass of phidaceaerepresents a primitive trait retained mosses, consistingof a singlefamily, the Tetra- from an ancestor in common among the Te- phidaceae Schimp., and two genera, Tetraphis traphidae, Sphagnidae,and Andreaeidae. Hedw. and TetrodontiumSchwaegr. Tetraphis It is the structureof the peristome that has is comprisedoftwo species, T.pellucida Hedw. been most frequently cited as evidence for a and T. geniculata Girg. ex Milde, and Tetro- primitive phylogenetic position for the Tetra- dontium is a monotypic genus erected for T. phidae. The peristome in both Tetraphisand brownianum (Dicks.) Schwaegr. All three Tetrodontiumconsists of four massive teeth species of the Tetraphidaeare north-temperate that fill the opercularregion of the maturecap- in distribution. sule. The teeth are nematodontous in that they Although there are no serious taxonomic are made up of whole, thick-walledcells, rather problemsat the specificlevel within the Tetra- than just remnants of cell walls, as in arthro- phidae, the phylogeneticand taxonomic status dontous peristomes. of the subclass has been disputed through the Moss peristomes can be classified as arthro- years. Many bryologists have expressed the dontous or nematodontous on the basis of view that the Tetraphidaeretain a significant comparative morphology without necessarily number of features that are primitive in the making hypotheses about the phylogenetic re- true mosses. The protonema of species in the lationshipbetween the two types ofperistomes. Tetraphidaceaehas thalloid "flaps" that are When Philibert (1884) distinguished arthro- often compared to the thalloid protonema of dontous and nernatodontous peristomes, he Sphagnum L. and Andreaea Hedw. (e.g., compared them in terms of cellular structure Campbell, 1905; Goebel, 1905; Schofield, and the patterns of lines on their inner and 1985). Although homology between the thal- outer surfaces.The morphological distinction loid protonema in these groups has not been is a phenetic and not a phylogenetic one, al- explicitly hypothesized, the suggestion, or at though Philibert and many other bryologists least the possibility, of homology is implicit in since have attached phylogenetic significance the frequentcomparisons that have been made. to the differencesin morphology. It is, however, still an open question as to Fundamentalsimilarities in the basic ground whether the thalloid protonema of the Tetra- plan among superficiallydivergent arthrodon- tous peristomes have led many bryologists to the interpretationthat mosses having arthro- 'Received for publication 3 June 1987; revision ac- dontous peristomesare monophyletic. That is, cepted 1 October 1987. basic similarities suggest to many that the ar- 2 Present address:Department of Biology, Ithaca Col- throdontous peristome has evolved only once lege, Ithaca, NY 14850. in the mosses. These fundamentalfeatures in- This researchwas supportedby NSF Grant No. BSR- 8506992. We thankB. D. Mishlerfor assistancewith field clude the formation of teeth from adjacent work and for commentingon an earliermanuscript draft. periclinalwalls ratherthan whole cells, the ar- We also thank M. Tumer for his able technicalassistance. ticulated appearance resulting from the pat- 1019 1020 AMERICAN JOURNAL OF BOTANY [Vol. 75 tems of lines on the inner and outer surfaces, *stometeeth in this species to published se- and the uniform number of cells in the outer quencesfor species in other subclassesof moss- and primaryperistomial layers throughoutar- es. In particular,we have sought to answerthe throdontousmosses. Anatomical studies have following questions during the course of our shown that almost all arthrodontous mosses study: 1) Is therea patternof development (i.e., have 32 cells in the outer peristomial layer a sequence of cell divisions) that is unique to (OPL) and 16 in the primaryperistomial layer and shared by the nematodontous peristomes (PPL) (Edwards, 1984; Shaw and Robinson, of species in the Polytrichidae and Tetraphi- 1984). Moreover, developmental studies, al- dae? 2) At what stage of development do Po- though rather few, indicate a remarkableuni- lytrichum-and Tetraphis-typeperistomes di- formity of development among arthrodontous verge? 3) At what stage of development do peristomes (Evans and Hooker, 1913; Tetraphis-typeand arthrodontousperistomes Blomquist and Robertson, 1941; Saito and diverge? In order to make comparisons be- Shimoze, 1954; Saito, 1956). tween peristomedevelopment in Tetraphisand Edwards(1979) devised a convention, which that in other mosses, we will rely on published he termed the peristomial formula, to make reports by others, as well as on our own pub- comparisonsof the number of cells in the peri- lished (Shaw, Anderson, and Mishler, 1987) stomial layers of mosses easier. The formula and unpublished observations. A detailed re- lists the number of cells in each of the three view of peristome structureand development, layers, from the outside inward, in only one intended to serve as a backgroundand ratio- eighthof the capsule'scircumference. The peri- nale for this and our future contributions, was stomial formula of almost all arthrodontous provided in Shaw et al. (1987). mosses ranges from 4:2:2 to 4:2:14 (Edwards, 1984; Shaw and Robinson, 1984). That is, the MATERIALSAND METHODS- Tetraphis pel- OPL (outer peristomial layer) uniformly con- lucida is widespread across the boreal and sists of 32 cells and the PPL (primaryperisto- ,north-temperate regions of the Northern mial layer)of 16 cells, but the inner peristomial Hemisphere. In North America, it extends layer (IPL) ranges from 16 to 112 cells in cir- northwardinto the tundra of Alaska and the cumference.Most of this variation in the num- Yukon Territory,and southwardin the East to ber of cells in the IPL occurs between species; South Carolinaand Alabama and in the West within a given species the number of cells in to Arizona and California,where it occurs in all three layers is relatively constant. the mountains-(Crum and Anderson, 1981). A monophyleticorigin for groupshaving ne- Populations sampled for this study originated matodontous peristomes is less clear. If ne- in the Ap-palachianMountains of North Car- matodontousperistomes are primitive with re- olina, where T. pellucida is common -on rotten spect to arthrodontous peristomes, as many tree -stumps, logs, and on soil or rocks near bryologists assert (e.g., Cavers, 1911; Dixon, streams. Collection data for the populations 1924; Edwards, 1984; Schofield, 1985), then we sampled are as follows: Mitchell Co.: Roan the nematodontous structureitself cannot be Mt., Anderson and Mishler 24,533; Anderson evoked as evidence for monophyly. It would and O-Toole 24,71 . Voucher specimens are simply be a feature that is retained from a deposited in DUKE. Plants were collected dur- common ancestor. Furthermore,the two sub- ing autumn and midwinter when