Phyllophora membranifolia, from Crouan & Crouan (1852).

Belongs within: Rhodophyta.
Contains: Nemaliophycidae, Corallinales, Ceramiales, Gracilariales, Plocamiaceae, Halymeniales, Rhodymeniales, Nemastomatales, Gigartinales, Gelidiales.

The Florideophycidae are a clade of multicellular red algae that ancestrally exhibit a triphasic life cycle (Adl et al. 2019).

Little discs of doom
Published 7 June 2007

Okay, total hyperbole in the title, but I wanted to get your attention. Today I’ll be looking at Pihiella liagoraciphila, a very distinctive member of the red algae that was only described recently (Huisman et al. 2003).

Individuals of Pihiella liagoraciphila in close-up and growing on Liagora, from Huisman et al. (2003).

Pihiella is an endo/epiphyte found on members of the red algal family Liagoraceae, but not a parasite as far as I can tell (red algae are notable for the range of associations between different taxa, most interestingly the occurrence of what is call ‘adelphoparasitism’, where parasitic species are closely related to their hosts). It has a quite simple disc-shaped or subspherical morphology with rhizoids to attach it to the host and long hairs and trichogynes (hair-like appendages of the female carpogonia that catch the male gametes). Mature discs are very small, up to 400 μm in diametre and 150 μm thick, though the hairs can be up to 800 μm long. Specimens were first observed as long ago as 1858, but were interpreted as buds of the host plant. Authors thereafter disagreed as to whether the so-called ‘monosporangial discs’ were asexual reproductive organs of the host or an independent organism. All authors agreed that the discs were asexually reproductive.

Sexually reproductive organs on the discs weren’t recorded until 2003, when Huisman et al. established that the discs were indeed a separate organism from the host. Pihiella seems to lack the obscenely complicated triphasic life cycles of other red algae. As already mentioned, the carpogonia (sexual organs) possess a long hair-like trichogyne, and Huisman et al. did observe examples with spermatia (the aflagellate male sex cells) attached. Nevertheless, Huisman et al. were unable to conclude whether the mature sporangia observed were asexually produced monosporangia, sexually produced zygotosporangia, or both (I feel the last option seems most likely, but what do I know?). No carposporophytes or tetrasporangia were observed (see the link above to find out what these are).

The morphology of Pihiella was too distinct from any other red alga to be phylogenetically informative but Huisman et al. were able to assess the phylogeny molecularly. Pihiella turned out to be quite isolated from other red algae, enough that Huisman et al. established a new monotypic order for it. Interestingly, the trees recovered Pihiella as sister taxon to Ahnfeltia, another phylogenetically isolated taxon, with a high level of support. Morphologically, Ahnfeltia is very distinct from Pihiella, being a large cartilaginous plant with a triphasic life cycle found in cool waters (the host family of Pihiella, Liagoraceae, is a mostly warm-water group). Though Ahnfeltia and Pihiella are each other’s closest relatives, the relationship is not close. Liagoraceae, in contrast, was in a quite distant part of the tree.

A parasite in the family
Published 7 June 2007

I mentioned in passing above the interesting phenomenon of adelphoparasitism, where a parasite is very closely related phylogenetically to its host. Since then, I’ve been wondering how such a situation arose, and specifically whether there was a connection between red algal adelphoparasitism and the complexities of red algal life cycles.

Life cycle of Chondrus crispus, from Wikimedia Commons.

Red algae fall into three to seven classes: Rhodellophyceae (which Yoon et al. 2006, divide into five), Bangiophyceae and Florideophyceae. Rhodellophyceae are unicellular, and I confess I don’t know the details of their life cycles. Bangiophyceae (which include Porphyra, the nori used in making sushi) alternate between distinct haploid and diploid generations. Florideophyceae include the vast majority of red algae, and verge on the completely insane in life style complexity. The basic florideophycean life cycle (which, as shown in the previous post, not all members of the class go through) involves no less than three alternating generations. Starting with the diploid tetrasporophyte, the tetrasporophyte releases haploid spores that settle and grow into gametophytes. Male gametophytes release spermatia (aflagellate sperm) that are captured by the female gametophytes and fertilise the carpogonia. The carpogonium (and this is the interesting part for this post) then grows into a carposporophyte, which remains attached to the parent gametophyte, releasing diploid spores that grow into new tetrasporophytes. So in effect, parasitism is already part of the florideophycean life cycle. Is it somehow possible that this parasitism is behind the rise of adelphoparasitism?

It’s worth noting here that similar patterns to “adelphoparasitism” are not unique to red algae. They have also been recorded among social Hymenoptera as well as mistletoes. Red algal parasites have traditionally been divided between adelphoparasites (which are closely related to their hosts) and alloparasites (not so closely related). The two classes are also supposedly distinguished by the mode of parasitism. In both, after the parasite rhizoid invades the host it adheres to and fuses with the host cells, injecting parasite nuclei and mitochondria. In adelphoparasites, the parasite nuclei then multiply within the host cell, hijacking it and causing the formation of growths which release spores of the parasite species (Goff et al., 1997), In alloparasites, the parasite nuclei do not divide in the host cytoplasm, though they do alter its physiology to facilitate the transfer of nutrients from host to parasite, and (I assume) the parasite reproductive bodies grow from the parasite rhizoid itself. Goff et al. (1997) demonstrated that one ‘genus’ of adelphoparasites had actually arisen polyphyletically from the host ‘genus’. Zuccarello et al. (2004) demonstrated the same thing for a ‘family’ of alloparasites. The latter authors therefore suggested that the terms ‘adelphoparasite’ and ‘alloparasite’ were not useful. However, this does still leave the question of the different cytoplasmic interactions (Zuccarello et al. implied that this might be due to the taxa studied belonging to different orders).

Goff et al. (1997) give two possible scenarios for the origin of parasitic red algae. In one, the parasites are ancestrally epiphytic, later becoming endophytic and eventually parasitic. In the second, the parasites derive directly from spores that lose the ability to survive independently of the parent. The existence of the carposporophyte, in my opinion, gives a lot of support to this option. One possibility is that adelphoparasites arose by the second method while alloparasites arose by the first.

Goff et al. also examined the main complaint towards the second origin—even if some mutant parasitic individual does arise, what is to stop it backcrossing to the parent population? How does the parasite become established as a new species? At present, there is no really satisfying answer to this question. Goff et al. point out that parasitic taxa have life cycles taking a fraction of the time of the host species. At any given time, only a small percentage of the individuals in a population of algae are reproductive—perhaps the difference in timing of life cycles simply meant that the chance of backcrossing between parasite and non-parasite was too low to prevent speciation?

Systematics of Florideophycidae

Characters (from Adl et al. 2019): Pluricellular with Golgi–ER/mitochondrion; growth by means of apical cells and lateral initials forming branched filaments in which cells are linked throughout by pit connections; life history fundamentally triphasic consisting of gametophytic, carposporophytic and tetrasporophytic phases; reproductive cells (monosporangia, spermatangia, carposporangia, tetrasporangia) generally terminal or lateral on filaments; carpogonia terminal or lateral, bearing an apical extension, the trichogyne, to which spermatangia attach; carposporophyte developing directly from carpogonium or its derivative.

Florideophycidae (see below for synonymy)AS12
    |  i. s.: Grania (Rosenvinge 1909) Kylin 1944HS02
    |           `--*G. efflorescensHS02
    |         Thallophyca Zhang 1989EB93, G03
    |           |--T. corrugata Zhang & Yuan 1992X04
    |           `--T. ramosa Zhang 1989X04
    |         Polyides [Spongiocarpeae]G64
    |           |--P. durvillaei Bory de Saint-Vincent 1828BS-V28
    |           `--P. rotundusG64
    |  `--CorallinophycidaeAS12
    |       |--CorallinalesHSA03
    |       `--Rhodogorgon [Rhodogorgonales]HSA03
    |            `--R. carriebowensisHSA03
    |--Hildenbrandiaceae [Hildenbrandiales, Hildenbrandiophycidae]HSA03
    |    |--ApophlaeaAB19
    |    |    |--A. lyallii Hooker & Harvey 1855L27
    |    |    `--A. sinclairii Harvey 1855L27
    |    `--Hildenbrandia Nardo 1834AS12
    |         |--H. occidentalis Setchell in Gardner 1917K98
    |         |--H. rivularisMS02
    |         |--H. rosea Kützing 1843S57
    |         `--H. rubra (Sommerfelt) Meneghini 1941 [=Verrucaria rubra Sommerfelt 1826; incl. H. prototypus Nardo 1834]K98
    `--+--Rhodymeniophycidae [Gastrocarpeae, Gongylospermeae, Laurenciaceae, Nemastomeae]AS12
       |    |  i. s.: Furcellaria fastigiataG64
       |    |         CaulacanthaceaeHS14
       |    |           |--Caulacanthus spinellus (Hooker & Harvey) Kützing 1849L27
       |    |           `--CatenellaHS14
       |    |                |--C. nipae Zanardini 1872HS14
       |    |                |--C. oligarthra Agardh 1876L27
       |    |                `--C. opuntia (Good & Woodw.) Greville 1830L27
       |    |                     |--C. o. var. opuntiaL27
       |    |                     `--C. o. var. fusiformis Agardh 1876L27
       |    |--CeramialesHSA03
       |    `--+--GracilarialesHSA03
       |       `--+--PlocamiaceaeHSA03
       |          |--+--HalymenialesHSA03
       |          |  `--RhodymenialesHSA03
       |          `--+--NemastomatalesHSA03
       |             `--+--GigartinalesHSA03
       |                `--+--GelidialesHSA03
       |                   `--Bonnemaisoniaceae [Bonnemaisoniales, Bonnemaisonieae]HSA03
       |                        |--Ptilonia magellanica (Montagne) Agardh 1852L27
       |                        |--Delisea Lamour. 1819L27, KC01
       |                        |    |--D. elegans (Agardh) Hooker & Harvey 1844L27
       |                        |    `--D. pulchra (Greville) Montagne 1844L27
       |                        |--BonnemaisoniaHSA03
       |                        |    |--B. asparagoidesG64
       |                        |    |--B. hamiferaHSA03
       |                        |    `--B. nootkana (Esper) Silva 1953S57
       |                        `--Asparagopsis Montagne 1841HL09
       |                             |--A. armata Harvey 1855L27
       |                             |--A. sandfordiana Harvey 1855L27
       |                             `--A. taxiformis (Delile) Trevisan 1845 [=Fucus taxiformis Delile 1813]HL09
            |--Pihiella Huisman, Sherwood & Abbott 2003 [Pihiellaceae, Pihiellales]HSA03
            |    `--*P. liagoraciphila Huisman, Sherwood & Abbott 2003HSA03
            `--Phyllophoraceae [Ahnfeltiales, Tylocarpeae]HSA03
                 |    |--S. californica Harvey 1841S57
                 |    `--S. interrupta (Agardh) Montagne 1846L27
                 |    |--G. crenulatusW03
                 |    |--G. griffithsiaeG64
                 |    |--G. nodiferus (Agardh) Agardh 1877 [=G. furcellatus var. nodiferus]L27
                 |    |--G. norvegicus (Gunner) Agardh 1851S57 [=Chondrus norvegicusG64]
                 |    `--G. platyphyllus Gardner 1927S57
                 |    |--A. concinna Agardh 1847S57
                 |    |--A. furcata (Hooker & Harvey) Agardh 1876L27
                 |    |--A. plicata (Hudson) Fries 1835S57 [=Gymnogongrus plicatusG64]
                 |    |--A. tobuchiensisTPG10
                 |    `--A. torulosa (Hooker & Harvey) Agardh 1876L27
                      |  i. s.: P. nervosaPP64
                      |--P. (sect. Phyllophora) rubensG64
                      |--P. (sect. Coccotylus) brodieiG64
                      `--P. sect. PhyllotylusG64
                           |--P. membranifoliaG64
                           `--P. palmelloidesG64

Florideophycidae [Desmiospermeae, Florideae, Floridei, Floridiaceae, Florideophyceae, Floridiophycidae, Halymeniae, Rhodospermeae]AS12

*Type species of generic name indicated


[AB19] Adl, S. M., D. Bass, C. E. Lane, J. Lukeš, C. L. Schoch, A. Smirnov, S. Agatha, C. Berney, M. W. Brown, F. Burki, P. Cárdenas, I. Čepička, L. Chistyakova, J. del Campo, M. Dunthorn, B. Edvardsen, Y. Eglit, L. Guillou, V. Hampl, A. A. Heiss, M. Hoppenrath, T. Y. James, A. Karnkowska, S. Karpov, E. Kim, M. Kolisko, A. Kudryavtsev, D. J. G. Lahr, E. Lara, L. Le Gall, D. H. Lynn, D. G. Mann, R. Massana, E. A. D. Mitchell, C. Morrow, J. S. Park, J. W. Pawlowski, M. J. Powell, D. J. Richter, S. Rueckert, L. Shadwick, S. Shimano, F. W. Spiegel, G. Torruella, N. Youssef, V. Zlatogursky & Q. Zhang. 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. Journal of Eukaryotic Microbiology 66: 4–119.

[AS12] Adl, S. M., A. G. B. Simpson, C. E. Lane, J. Lukeš, D. Bass, S. S. Bowser, M. W. Brown, F. Burki, M. Dunthorn, V. Hampl, A. Heiss, M. Hoppenrath, E. Lara, E. Le Gall, D. H. Lynn, H. McManus, E. A. D. Mitchell, S. E. Mozley-Stanridge, L. W. Parfrey, J. Pawlowski, S. Rueckert, L. Shadwick, C. L. Schoch, A. Smirnov & F. W. Spiegel. 2012. The revised classification of eukaryotes. Journal of Eukaryotic Microbiology 59 (5): 429–493.

[BS-V28] Bory de Saint-Vincent, J. B. 1828. Voyage Autour du Monde, Exécuté par Ordre du Roi, Sur la Corvette de Sa Majesté, La Coquille, pendant les années 1822, 1823, 1824 et 1825. Botanique. Cryptogamie. Arthus Bertrand: Paris.

[EB93] Edwards, D., J. G. Baldauf, P. R. Brown, K. J. Dorning, M. Feist, L. T. Gallagher, N. Grambast-Fessard, M. B. Hart, A. J. Powell & R. Riding. 1993. ‘Algae’. In: Benton, M. J. (ed.) The Fossil Record 2 pp. 15–40. Chapman & Hall: London.

[G03] Gnilovskaya, M. B. 2003. The oldest tissue differentiation in Precambrian (Vendian) algae. Paleontologicheskii Zhurnal 2003 (2): 92–98 (translated: Paleontological Journal 37 (2): 196–204).

Goff, L. J., J. Ashen & D. Moon. 1997. The evolution of parasites from their hosts: a case study in the parasitic red algae. Evolution 51 (4): 1068–1078.

[G64] Gray, J. E. 1864. Handbook of British Water-weeds or Algae. R. Hardwicke: London.

[HS02] Harper, J. T., & G. W. Saunders. 2002. A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta). European Journal of Phycology 37: 463–476.

[HL09] Huisman, J. M., F. Leliaert, H. Veerbruggen & R. A. Townsend. 2009. Marine benthic plants of Western Australia’s shelf-edge atolls. Records of the Western Australian Museum Supplement 77: 50–87.

[HS14] Huisman, J. M., & A. Sampey. 2014. Kimberley marine biota. Historical data: marine plants. Records of the Western Australian Museum Supplement 84: 45–67.

[HSA03] Huisman, J. M., A. R. Sherwood & I. A. Abbott. 2003. Morphology, reproduction, and the 18S rRNA gene sequence of Pihiella liagoraciphila gen. et sp. nov. (Rhodophyta), the so-called ‘monosporangial discs’ associated with members of the Liagoraceae (Rhodophyta), and proposal of the Pihiellales ord. nov. Journal of Phycology 39: 978–987.

[K98] Kaehler, S. 1998. The non-coralline epilithic encrusting algae of Hong Kong II: additions and identification. Asian Marine Biology 15: 1–17.

[KC01] Kirk, P. M., P. F. Cannon, J. C. David & J. A. Stalpers. 2001. Ainsworth & Bisby’s Dictionary of the Fungi 9th ed. CAB International: Wallingford (UK).

[L27] Laing, R. M. 1927. A reference list of New Zealand marine algae. Transactions and Proceedings of the New Zealand Institute 57: 126–185.

[MS02] Müller, K. M., A. R. Sherwood, C. M. Pueschel, R. R. Gutell & R. G. Sheath. 2002. A proposal for a new red algal order, the Thoreales. Journal of Phycology 38: 807–820.

[S57] Scagel, R. F. 1957. An annotated list of the marine algae of British Columbia and northern Washington (including keys to genera). National Museum of Canada Bulletin 150: 1–289.

[TPG10] Trebukhova, Y. A., O. N. Pavlyuk & V. V. Galtsova. 2010. Community of free-living marine nematodes on macrophytes (Starka Strait, Peter the Great Bay, Sea of Japan). In: China-Russia Bilateral Symposium: Proceedings of the China-Russia Bilateral Symposium of “Comparison on Marine Biodiversity in the Northwest Pacific Ocean”, 10–11 October 2010, Qingdao (China) pp. 149–153. Institute of Oceanology, Chinese Academy of Sciences; A. V. Zhirmunsky Institute of Marine Biology, Far East Branch of the Russian Academy of Sciences.

[W03] Womersley, H. B. S. 2003. The Marine Benthic Flora of southern Australia. Rhodophytapart IIID. CeramialesDelesseriaceae, Sarcomeniaceae, Rhodomelaceae. Flora of Australia Supplementary Series 18. Australian Biological Resources Study: Canberra, and the State Herbarium of South Australia: Adelaide.

[X04] Xiao, S. 2004. New multicellular algal fossils and acritarchs in Doushantuo chert nodules (Neoproterozoic; Yangtze Gorges, south China). Journal of Paleontology 78 (2): 393–401.

Zuccarello, G. C., D. Moon & L. J. Goff. 2004. A phylogenetic study of parasitic genera placed in the family Choreocolacaceae (Rhodophyta). Journal of Phycology 40: 937–945.

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