Belongs within: Rhodophyta.
Contains: Nemaliophycidae, Corallinales, Ahnfeltiophycidae, Ceramiales, Gracilariales, Plocamiaceae, Halymeniales, Rhodymeniales, Nemastomatales, Gigartinales, Gelidiales.
The Florideophycidae are a clade of multicellular red algae that ancestrally exhibit a triphasic life cycle. Cells are linked by pit connections with basal lineages often being distinguishable by the features of these connections (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).
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.
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 (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
|--+--NemaliophycidaeHSA03
| `--CorallinophycidaeAS12
| |--CorallinalesHSA03
| `--Rhodogorgon [Rhodogorgonales]HSA03
| `--R. carriebowensisHSA03
|--Hildenbrandiaceae [Hildenbrandiales, Hildenbrandiophycidae]HSA03
| |--ApophlaeaAB19
| | |--A. lyallii Hooker & Harvey 1855L27
| | `--A. sinclairii Harvey 1855L27
| `--Hildenbrandia Nardo 1834AS12 (see below for synonymy)
| |--H. dawsonii (Ardré) Hollenberg 1971 [=H. canariensis var. dawsonii Ardré 1959]AH76
| |--H. occidentalis Setchell in Gardner 1917K98
| |--H. rivularisMS02
| `--H. rubra (Sommerfelt) Meneghini 1941K98 (see below for synonymy)
`--+--AhnfeltiophycidaeAS12
`--Rhodymeniophycidae [Gastrocarpeae, Gongylospermeae, Laurenciaceae, Nemastomeae]AS12
| i. s.: FurcellariaceaeS80
| |--Furcellaria fastigiataG64
| `--Neurocaulon Zanardini ex Kützing 1849 (nom. cons.)S80
| `--*N. foliosum (Meneghini) Zanardini ex Kützing 1849S80 (see below for synonymy)
| 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
|--Asparagopsis Montagne 1841HL09
| |--A. armata Harvey 1855L27
| |--‘Polysiphonia’ hillebrandii Ardissone 1883 (see below for synonymy)AH76
| |--A. sandfordiana Harvey 1855L27
| `--A. taxiformis (Delile) Trevisan 1845 [=Fucus taxiformis Delile 1813]HL09
`--Bonnemaisonia Agardh 1822AH76
|--B. asparagoidesG64
|--B. geniculata Gardner 1927AH76
|--B. hamifera Hariot 1891AH76
|--‘Trailliella’ intricata Batters 1896AH76
`--B. nootkana (Esper) Silva 1953 (see below for synonymy)AH76
Bonnemaisonia nootkana (Esper) Silva 1953 [=Fucus nootkanus Esper 1802; incl. B. californica Buffham 1896]AH76
Florideophycidae [Desmiospermeae, Florideae, Floridei, Floridiaceae, Florideophyceae, Floridiophycidae, Halymeniae, Rhodospermeae]AS12
Hildenbrandia Nardo 1834AS12 [=HildbrandtiaS80, Hildebrandtia (l. c.) nec Nieden 1907 (ICZN) nec Olsoufieff 1938 (ICZN)S80, Hildenbrandtia (l. c.)S80]
Hildenbrandia rubra (Sommerfelt) Meneghini 1941K98 [=Verrucaria rubra Sommerfelt 1826K98; incl. *H. prototypus Nardo 1834S80, K98, H. rosea Kützing 1843AH76]
*Neurocaulon foliosum (Meneghini) Zanardini ex Kützing 1849S80 [=Iridaea foliosa Meneghini 1841S80, Nevrocaulon foliosumS80; incl. Cryptonemia forbesii Harvey in Hooker 1844S80, Fucus reniformis Turner 1809S80, Callymenia reniformisS57, Constantinea reniformis (Turner) Postels & Ruprecht 1840S80, Euhymenia reniformis (Turner) Kützing 1849S80, Halymenia reniformis (Turner) Agardh 1817S80, Iridaea reniformis (Turner) Greville 1830S80, Kallymenia reniformis (Turner) Agardh 1842S80, Neurocaulon reniforme Schmitz 1889S80, Rhodomenia reniformis (Turner) Hooker 1833S80, Sphaerococcus reniformis (Turner) Agardh 1817S80]
‘Polysiphonia’ hillebrandii Ardissone 1883 [=Falkenbergia hillebrandii (Ardissone) Falkenberg 1901]AH76
*Type species of generic name indicated
References
[AH76] Abbott, I. A., & G. J. Hollenberg. 1976. Marine Algae of California. Stanford University Press.
[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.
[S80] Silva, P. C. 1980. Remarks on algal nomenclature VI. Taxon 29 (1): 121–145.
[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.