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Hidden Diversity and Cryptic Speciation Refute Cosmopolitan Distribution in Caprella Penantis (Crustacea: Amphipoda: Caprellidae)

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Hidden Diversity and Cryptic Speciation Refute Cosmopolitan Distribution in Caprella Penantis (Crustacea: Amphipoda: Caprellidae) Accepted on 14 November 2012 © 2013 Blackwell Verlag GmbH J Zoolog Syst Evol Res doi: 10.1111/jzs.12010 1Laboratorio de Biología Marina, Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Seville Spain; 2Museo Nacional de Ciencias Naturales (MNCN, CSIC), Madrid Spain; 3 Present address: Department of Biology, Brigham Young University, 401 Widtsoe Building,Provo UT, 84602, USA Hidden diversity and cryptic speciation refute cosmopolitan distribution in Caprella penantis (Crustacea: Amphipoda: Caprellidae) 1 2,3 2 1 MARÍA PILAR CABEZAS ,PATRICIA CABEZAS ,ANNIE MACHORDOM and JOSÉ M. GUERRA-GARCÍA Abstract Caprella penantis is considered a cosmopolitan species and one of the most challenging caprellids in taxonomic terms because of its remarkable intra- specific morphological variation. This study examined DNA sequences from mitochondrial (COI) and nuclear (18S) markers together with morphologi- cal data from 25 localities of C. penantis, and closely related species Caprella dilatata and Caprella andreae, all traditionally considered part of the old ‘acutifrons’ complex. The large genetic divergence and reciprocally allopatric distributions point to the existence of a species complex of at least four species, of which one is reported as a cryptic species. This study provides the first evidence of cryptic speciation in the family Caprellidae, and questions the validity of some traditional morphological characters used to delimit species in the genus Caprella. Our results are consistent with the idea that main factors were probably isolation by distance and ecological traits, promoting diversification in C. penantis. The strong genetic structure reported for this species in the Iberian Peninsula and Moroccan coasts also suggests restriction to dispersal as well as the presence of refugial areas. These results highlight the utility of the COI and 18S genes in combination with morphological characters for shedding light on systematic questions in caprellids, and patterns of genetic connectivity. Key words: COI – cryptic species – genetic structure – morphology – 18S – taxonomy Introduction gammarids (e.g. Hogg et al. 2006; Witt et al. 2006; Seidel et al. 2009; Pilgrim and Darling 2010; Baird et al. 2011). Particularly Scientists have long been interested in understanding the ecologi- interesting is the species Caprella penantis Leach, 1814 (Crus- cal and evolutionary processes underlying the origin, distribution tacea, Amphipoda, Caprellidae), which despite its limited power and preservation of biological diversity, with increasing attention of dispersal, is considered to have a cosmopolitan distribution during recent years because of the enormous loss of worldwide covering tropical, subtropical and temperate oceans (McCain diversity (Costello et al. 2010). Mitigation measures are required, 1968; Vassilenko 1991; Krapp-Schickel 1993). Caprella penan- but difficulties arise due to the unknown extent of biodiversity tis constitutes one of the dominant caprellid species in intertidal and spatial distribution of species assemblages (Witt et al. 2006; communities and shallow waters in marine ecosystems (Guerra- Radulovici et al. 2009), as well as the difficulty describing spe- García 2001; Guerra-García et al. 2009b,c; Guerra-García and cies based solely on morphological characters (Knowlton 1993; Izquierdo 2010), and an important dietary component for many Remerie et al. 2006; Beheregaray and Caccone 2007). In the coastal marine fish species (Caine 1989; Woods 2009). It can marine environment, this fact is even more remarkable because À reach densities higher than 10 000 individuals m 2 in intertidal genetic and ecological studies frequently highlight the existence seaweeds of temperate ecosystems (Guerra-García et al. 2009c, of cryptic species (Knowlton 1993, 2000; Mathews 2006; Calvo d, 2010a; Guerra-García and Izquierdo 2010) and can go et al. 2009): species that are genetically distinct, but difficult to À beyond 50 000 individuals m 2 in other marine habitats (see distinguish using morphological characters (Mayr 1948, 1963; Takeuchi 1999). Moreover, it has recently been considered a Mayr and Ashlock 1991). Unclear species boundaries and cryptic sensitive species (Guerra-García and García-Gomez 2001) as speciation are common problems in a wide range of marine well as a good biomonitor of trace metal contamination in these organisms (Knowlton 1993; Avise 1994; Witt et al. 2006). ecosystems, even better than other marine invertebrates (Guerra- Establishing species boundaries, involving the identification of García et al. 2009a, 2010b). Despite its abundance, cosmopoli- cryptic species, is fundamentally important in biodiversity assess- tan distribution and importance as bioindicator, the taxonomy of ment (Knowlton 1993, 2000; Cook et al. 2008) and in subse- C. penantis remains unsettled (Mayer 1890, 1903; McCain and quent conservation strategy design (Bickford et al. 2007). Steinberg 1970). The taxonomy status of this species has been Reliance on morphology-based taxonomy alone might critically fraught with controversy for years, and it has been recorded underestimate biodiversity. Consequently, combination of multi- under several species or subspecies names from temperate ple types of independent sources of data, including molecular, regions worldwide (McCain and Steinberg 1970) because of its morphological and ecological data, is required to accurately considerable intraspecific morphological variability (McCain assess species boundaries (Remerie et al. 2006; Roe and Sperling 1968; Laubitz 1972; Guerra-García et al. 2006; Cabezas et al. 2007; Hou and Li 2010). 2010). In his monographs, Mayer (1890, 1903) described 19 Among crustaceans, the order Amphipoda is one of the most forms of the ‘Caprella acutifrons’ group. Several of these forms problematic taxonomic groups because of the difficulty to iden- have already been given specific rank (Utinomi 1943; Dougher- tify diagnostic characters (Martin and Davis 2001; Browne ty and Steinberg 1953; Vassilenko 1967; Laubitz 1972). For et al. 2007), and cryptic speciation has been widely reported for example, form andreae was assigned to Caprella andreae Mayer, 1890 (McCain 1968); forms typica and minor have been Corresponding author: María Pilar Cabezas Rodríguez ([email protected]) assigned to Caprella dilatata Krøyer, 1843 (McCain 1968) and Contributing authors: Patricia Cabezas ([email protected]), probably forms tabida and tibada also belong to this species, Annie Machordom ([email protected]), Jose M. Guerra-García although their taxonomic status under C. penantis is still under ([email protected]) J Zoolog Syst Evol Res (2013) 51(2), 85--99 86 CABEZAS,CABEZAS,MACHORDOM and GUERRA-GARCÍA discussion (Guerra-García et al. 2006). Forms gibbosa, carolin- code and coordinates for the sampling localities, as well as some collec- ensis, virginia, lusitanica, testudo and simulatrix are still classi- tion information are summarized in Table 1. fied under the species C. penantis (McCain 1968; Laubitz 1970, 1972; Krapp-Schickel 1993), characterized mainly by the pres- Morphological analyses ence of short and triangular rostrum on the front of the head, second gnathopods with proximal poison tooth and pereopods 5 All individuals were morphologically identified by stereomicroscope –7 propodi palm slightly concave with proximal grasping according to the characters described by Mayer (1882, 1890, 1903) and spines. Under this framework, it is clear that more comprehen- Krapp-Schickel (1993). Only adult males were considered, as most of the fi sive studies are urgently needed to distinguish between intra- species-speci c diagnostic characters are fully developed and more obvious in these specimens. We particularly examined male gnathopods, gill shape, and interspecific variability within C. penantis. robustness of antenna 1, concavity/convexity of propodi palm in pereopods Like all peracarid crustaceans, the dispersion of C. penantis is 5–7 (P5-7), presence/absence of ‘grasping spines’ and body length. assumed to be primarily driven by rafting (Thiel 2002; Thiel et al. 2003b) because of the lack of a planktonic larval stage (Thiel and Vasquez 2000; Cook et al. 2004) and limited swim- DNA extraction, PCR amplification and sequencing ming capabilities (Thiel et al. 2003b). Thus, considerable genetic Genomic DNA was extracted from legs, gnathopods, gills and pereopods differentiation among populations and the existence of cryptic except when individuals were too small (in those cases, the whole speci- species is expected. Here, we present the first study to clarify men was used) using the BioSprint 15 DNA Blood Kit (45) (Qiagen the taxonomic status of the species C. penantis as well as evalu- Iberia, Madrid, Spain). Protocol was carried out according to the manu- ate genetic connectivity patterns in relation to life history and facturer’s instructions, but with elution volume decreased to 100 llto ecological traits. For this purpose, we examined genetic variabil- maximize DNA concentration. Final DNA concentration was estimated ity in mitochondrial and nuclear genes together with morphologi- using a Nanodrop Spectrophotometer (Nanodrop 1000: Thermo Scientific, cal characters in 30 populations across its cosmopolitan Madrid, Spain). distribution. An approximately 1200-base pair (bp) fragment of the mitochondrial DNA (mtDNA) cytochrome c oxidase subunit 1 gene (COI) was ampli- fied in two overlapping PCR fragments of 550 and 660 bp respectively. Material and methods Because of the poor amplification
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