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Evolutionary Reversals in Bossiella (Corallinales, Rhodophyta): First Report of a Coralline Genus with Both Geniculate and Nongeniculate Species1

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Evolutionary Reversals in Bossiella (Corallinales, Rhodophyta): First Report of a Coralline Genus with Both Geniculate and Nongeniculate Species1 J. Phycol. 54, 788–798 (2018) © 2018 Phycological Society of America DOI: 10.1111/jpy.12788 EVOLUTIONARY REVERSALS IN BOSSIELLA (CORALLINALES, RHODOPHYTA): FIRST REPORT OF A CORALLINE GENUS WITH BOTH GENICULATE AND NONGENICULATE SPECIES1 Katharine R. Hind 2 Department of Botany and Beaty Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4 Hakai Institute, Pruth Harbour, Calvert Island, British Columbia V0P 1H0, Canada Paul W. Gabrielson Biology Department and Herbarium, University of North Carolina Chapel Hill, Coker Hall CB 3280, Chapel Hill, North Carolina, 27599-3280, USA Cassandra Jensen Department of Botany and Beaty Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4 and Patrick T. Martone Department of Botany and Beaty Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4 Hakai Institute, Pruth Harbour, Calvert Island, British Columbia V0P 1H0, Canada This is the first report of a coralline genus with both Abbreviations: BC, British Columbia; BI, Bayesian geniculate (upright fronds with non-calcified joints) inference; BS, bootstrap; CA, California; COI-5P, cy- and nongeniculate species that has been verified by tochrome c oxidase subunit 1-five prime; ML, maxi- DNA sequence data. Two nongeniculate (crustose) mum likelihood; mya, million years ago; PP, species of Bossiella are recognized, B. mayae sp. nov. posterior probability; WA, Washington and B. exarticulata sp. nov. DNA sequencing of the lectotype specimen of Pseudolithophyllum whidbeyense revealed that this name had been misapplied and Evolutionary reversals occur when a derived char- instead belongs to an undescribed coralline species in acter state reflects the phenotype of an ancestral lin- the Hapalidiales. Phylogenetic analyses of eage (Porter and Crandall 2003). The mechanism concatenated DNA sequences (psbA, rbcL, COI-5P) for evolutionary reversals and the most parsimo- indicate that B. mayae and B. exarticulata represent nious explanation for their occurrence is the sec- phenotypic reversals from the geniculate character ondary loss of a trait that was previously gained by state back to the nongeniculate character state. an ancestral lineage. Secondary loss is the most Secondary loss of genicula has occurred three times in likely explanation for an evolutionary reversal when the subfamily Corallinoideae, once to generate the character state changes are infrequent and when entirely nongeniculate genus Crusticorallina and twice the lineage exhibiting secondary loss is embedded in the now morphologically heterotypic Bossiella.Since within a clade of organisms where the trait is pre- phenotypic reversals have occurred several times sent (Wiens 2001). With the advent of molecular sys- during the evolution of coralline algae, we speculate tematics, we now have an independent data set, about the putative mechanism and adaptive DNA sequence data, to recognize and assess what significance of this phenomenon. appear to be phenotypic reversals (Porter and Cran- dall 2003). Key index words: Bossiella exarticulata; Bossiella mayae; Coralline algae (orders Corallinales, Hapalidiales, COI-5P; crustose coralline algae; cryptic species; and Sporolithales) are a group of red seaweeds psbA; Pseudolithophyllum whidbeyense; rbcL; secondary within subclass Corallinophycidae that have calcium loss; sequencing type specimens carbonate deposited in their cell walls, primarily as high Mg-calcite (Nash et al. 2011, 2016, Diaz-Pulido 1Received 30 October 2017. Accepted 16 July 2018. First Pub- et al. 2014). Two morphological character states lished 23 September 2018. Published Online 16 October 2018, Wiley occur in coralline red algae: geniculate corallines Online Library (wileyonlinelibrary.com). 2Author for correspondence: e-mail [email protected]. are typically erect with short, non-calcified segments Editorial Responsibility: C. Amsler (Associate Editor) (genicula) between larger calcified segments 788 EVOLUTIONARY REVERSALS IN BOSSIELLA 789 (intergenicula). Nongeniculate corallines are protuberances, and sometimes tessellate with semi- encrusting in habit or form rhodoliths and are pre- circular swirls (Steneck and Paine 1986). Upon dominately calcified (Johansen 1981). The Sporo- sequencing, these specimens proved to belong in lithales and Hapalidiales are comprised entirely of Bossiella (Corallinoideae), a genus of geniculate spe- nongeniculate corallines, whereas Corallinales con- cies with lateral conceptacles. We first assumed that tains both geniculate and nongeniculate taxa (Nel- we sequenced the encrusting base of one of the son et al. 2015). The fossil record has long geniculate species of Bossiella, as several species (no- suggested that nongeniculate corallines are ances- tably B. frondifera) have conspicuous and extensive tral to geniculate corallines (Johnson 1961, Wray crustose bases from which numerous erect axes 1977). Johansen (1969) and Cabioch (1971) hypoth- arise. However, the sequences did not match any esized that geniculate corallines arose from non- geniculate Bossiella in our databases, then or now. geniculate corallines several times because different Most convincing, however, were conceptacles found groups of geniculate corallines have different genic- within the crusts we had sequenced, clearly distin- ular anatomies. Johansen (1969: 43–44) suggested guishing these specimens from other Bossiella spe- that genicula evolved three times giving rise to the cies. Conceptacles have never been recorded from subfamilies Metagoniolithoideae, Amphiroideae, the crustose bases of geniculate corallines, including and Corallinoideae, but did not speculate from Bossiella, demonstrating that these specimens most which nongeniculate ancestors the three subfamilies likely represented nongeniculate species. Using of geniculate corallines arose. DNA sequences from two plastid (rbcL and psbA) Molecular phylogenies (Aguirre et al. 2010, Bit- and one mitochondrial (COI-5P) marker, we tner et al. 2011) have been congruent with the fossil demonstrate that two species belonging in Bossiella record indicating that nongeniculate corallines have lost their genicula; these nongeniculate species evolved earlier than geniculate corallines. DNA are described here as B. mayae sp. nov. and B. exar- sequence data have been used to infer which non- ticulata sp. nov. We also explain why the name geniculate lineages share a common ancestor with P. whidbeyense applies to a species of Hapalidiales geniculate lineages, lending insight into this and cannot be used for any Bossiella species. repeated evolutionary trend. Within Metago- History of Pseudolithophyllum. whidbeyense. The niolithoideae the geniculate genus Metagoniolithon is basionym of P. whidbeyense is Lithophyllum whidbeyense, sister to the nongeniculate genus Porolithon (Bittner originally described by Foslie (1906). Foslie (1906) et al. 2011, Kato et al. 2011, Rosler€ et al. 2016) and based his description of L. whidbeyense on two collec- within Lithophylloideae the geniculate genera tions sent to him by Nathaniel Lyon Gardner (NLG Amphiroa and Lithothrix are sister to the nongenicu- 655 and NLG 656), both from the west coast of late Lithophyllum (Bailey and Chapman 1998, Bailey Whidbey Island, WA, USA and all on limpet shells 1999, Gabrielson et al. 2011), but which nongenicu- (Acmaea mitra). Foslie (1906) described this new spe- late taxon is sister to Corallinoideae is unclear. cies as crustose, 0.3–1 mm thick, smooth, and Until 2013, Corallinoideae was characterized as weakly glossy with a hypothallus occupying 1/3–2/3 containing only geniculate taxa, but Hind and Saun- of the crust thickness and those cells 2–4 times ders (2013) documented the first evidence of sec- longer (12–25 up to 30 lm) than wide (6–10 lm). ondary loss of genicula in that subfamily. Using a Perithallial cells were subquadrate to vertically elon- molecular phylogenetic approach, they demon- gate (7–14 up to 18 lm long) and 6–10 lm wide. strated that the Northeast Pacific nongeniculate spe- Cystocarpic conceptacles were tightly packed, weakly cies then known as Pseudolithophyllum muricatum convex and 350–600 lm diameter. belonged in the Corallinoideae. Recently, Hind Mason (1953) added to the description that the et al. (2016) erected a new genus, Crusticorallina, for crust was “crowded with numerous closely crowded P. muricatum and related species. Although Metago- excrescences 2 mm high and 1–1.5 mm thick” and niolithoideae, Lithophylloideae, and Corallinoideae that specimens were also found on stones. Adey all contain geniculate and nongeniculate species, (1970) transferred the species to Mesophyllum as genera within each subfamily are defined as possess- M. whidbeyense, but expressed “considerable doubt” ing one or the other morphological character state about its generic placement as he had not seen bi- (Hind et al. 2016). The Corallinoideae offers an tetrasporangial conceptacles (Adey’s asexual concep- excellent system for studying secondary loss of tacles) and specimens had a Mesophyllum-like epi- genicula because this phenotypic reversion is rela- thallium and upper perithallium. Steneck and Paine tively infrequent and Crusticorallina is embedded (1986), based on numerous field collected speci- within a large clade of geniculate species. mens as well as an isolectotype specimen (UC In the early 2000s KRH and PWG collected non- 739464), provided a detailed description of the veg- geniculate corallines
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