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Reproductive Isolation and Morphological Divergence Between Cryptic Lineages of the Copepod Acartia Tonsa in Chesapeake Bay

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Reproductive Isolation and Morphological Divergence Between Cryptic Lineages of the Copepod Acartia Tonsa in Chesapeake Bay Reproductive isolation and morphological divergence between cryptic lineages of the copepod Acartia tonsa in Chesapeake Bay *L.V. Plough, C. Fitzgerald, A. Plummer, and J.J. Pierson Horn Point Laboratory, University of Maryland Center for Environmental Science, Horn Point Laboratory, Cambridge MD, 21613 *Corresponding author: [email protected] Running head: Reproductive isolation between cryptic copepod lineages Keywords: cryptic species, zooplankton, reproduction, copepod, food-web 1 1 Abstract 2 Recent advances in molecular technologies have revealed cryptic species across many 3 marine zooplankton taxa. However, the patterns and drivers of cryptic divergence are complex, 4 and few studies examine reproductive status among lineages through crosses. In this study, we 5 performed pair crosses within and between two deeply divergent (cryptic) lineages (named F 6 ‘Fresh’ and S, ‘Salt’) of the estuarine copepod Acartia tonsa from upper Chesapeake Bay, USA 7 examining egg production and hatching rate. We also examined differences in morphology 8 (prosome length) and chemical composition of the two lineages. Crossing experiments revealed 9 that egg production did not differ among cross types but hatching rate was significantly lower for 10 the between-lineage crosses (mean hatching rate of 0.02 for F×S vs. 0.46 and 0.52 for F×F and 11 S×S, respectively). The nearly complete lack of nauplii production for between-lineage crosses 12 suggests strong reproductive isolation, which supports previous molecular data. Significant 13 differences between the lineages in size (F lineage is 13-14% shorter) and chemical composition 14 (F lineages have 70% less Carbon per copepod) may indicate pre-zygotic barriers to reproduction 15 (e.g. morphological or gametic incompatibility). Overall, based on the crossing, morphological, 16 and chemical data reported here, and synthesizing previous biological data on the F and S 17 lineages, we suggest that these cryptic lineages are likely to be separate, reproductively isolated 18 species. Further work examining how divergent lineages of A. tonsa respond to environmental 19 change and how they differ in their quality as prey items will be important for understanding 20 trophic dynamics in estuarine environments like Chesapeake Bay. 21 22 23 2 24 Introduction 25 Understanding the patterns and drivers of biodiversity in the world’s oceans is a 26 fundamental area of research in marine ecology and biological oceanography (Hutchinson 1961), 27 with implications for geochemical cycling (Lotze et al. 2006, Lomas et al. 2014), food-web 28 dynamics (Turner et al. 2004, Duffy & Stachowicz 2006, Hughes et al. 2008), and the 29 productivity of fisheries (e.g., Beaugrand et al. 2002 2003). Central to this work is the accurate 30 quantification or delineation of species and species diversity, a process that has historically relied 31 on morphology but can be challenging in species-rich groups or for taxa that lack obvious or 32 reliable morphological characters (e.g. Hillis 1987, Knowlton 1993, Norris 2000, Bickford et al. 33 2007). Species diversity has been shown to vary substantially among marine fauna (e.g. Titensor 34 et al. 2010, but see Piejnenburg & Goetze 2013), but whether or not this is due to idiosyncratic 35 features of the biology and ecology of particular taxonomic groups, a lack of data, or bias in the 36 types of taxa examined is not always clear, and species diversity is likely to be substantially 37 underestimated across less studied marine fauna (Knowlton 1993, Bickford et al. 2007, 38 McManus & Katz 2009). 39 For holoplanktonic marine species residing in open and coastal oceans, the paradigm has 40 long been that the relative lack of observable species diversity (morphological conservatism) was 41 due to a combination of factors including the general lack of geographic barriers, strong ocean 42 currents, and poor swimming ability of plankton that results in high dispersal and high gene flow 43 over large ocean distances (e.g. Norris 2000, Goetze & Ohman 2010, Peijnenburg & Goetze 44 2013). Application of novel molecular genetic technologies over the last two decades has 45 challenged this view of the plankton, with studies repeatedly demonstrating substantial ‘un-seen’ 46 diversity and deep intra-specific genetic divergences among ‘populations’ of morphologically 3 47 static groups over ocean basin scales or even smaller distances (100s to 1000’s of km; e.g. Sáez 48 et al. 2006, Lee 2000, Bucklin et al. 1996, Halbert et al. 2013). It is now clear that sibling or 49 cryptic species (genetically divergent clades with similar or indistinguishable morphology) are 50 common among the plankton and zooplankton, having been identified in many pelagic phyla 51 including cnidaria (Holland et al. 2004, Scroth et al. 2002, Warner et al. 2015), foraminifera 52 (Darling &Wade 2008, Aurahs et al. 2009) coccolithophores (Sáez et al. 2003), pico-eukaryotes 53 (Slapeta et al. 2006), chaetognaths (Peijnenburg et al. 2006) and crustaceans (e.g. copepods; 54 Bucklin 1996, Lee et al. 2000, Chen & Hare 2008, Goetze & Ohman 2010, Halbert et al. 2013). 55 Varying degrees, rates, and geographic scales of divergence and diversity have been found 56 among and within zooplankton groups (Bickford et al. 2007, Peijnenburg & Goetze 2013, 57 Halbert et al. 2013), suggesting that the underlying drivers of species diversity are complex and 58 that general patterns may be hard to predict. Nevertheless, the existence of cryptic species within 59 such broad taxonomic groups within the plankton suggests even more species diversity than 60 previously thought, and zooplankters have a great propensity to adapt and evolve relatively 61 quickly in response to ecological and anthropogenic change (Peijnenburg & Goetze 2013). 62 Species diversity and morphological crypsis in copepods 63 Much research effort has recently been focused on the characterization of species 64 diversity in marine copepods, an ecologically significant group of small crustaceans with high 65 abundances and wide distribution among the world’s oceans and coastal seas (e.g. Beaugrand et 66 al. 2003, Turner et al. 2004, Calbet 2008). Previous genetic studies of open ocean copepod 67 species have revealed striking patterns of restricted gene flow on ocean-basin scales and that 68 many putative ‘cosmopolitan’ species are actually comprised of multiple, genetically distinct 4 69 lineages (e.g. Bucklin et al. 1996, Goetze & Ohman 2010, Halbert et al. 2013, Vinas et al. 2015). 70 Consistent with phylogeographic studies of other zooplankton, patterns and scales of divergence 71 appear to vary substantially among cryptic species groups, and sometimes in unpredictable ways. 72 For example, a circum-global phylogeographic survey of Eucalanoidea revealed that while 73 ocean basins often served as boundaries among cryptic lineages, the deeper relationships of sister 74 taxa did not correspond to geographic expectations at the hemispheric level or expectations 75 based on current patterns of ocean circulation (e.g. Rhinocalanus nasutus; Goetze & Ohman 76 2010). 77 Coastal and freshwater copepod species also show high levels of endemism and crypsis, 78 though sometimes at smaller geographic scales (e.g. Lee 2000, Lee & Frost 2002, Caudill & 79 Bucklin 2004, Marrone et al. 2013). For example, genetic analysis of Eurytemora affinis 80 populations across the US, Europe, and Asia have revealed eight sibling species with conserved 81 morphology, and crosses have further shown wide variation in the level of reproductive isolation 82 among ‘populations’ (Lee 2000). Interestingly, reproductive success was greatest among two of 83 the more genetically distant clades, suggesting weak correlation between reproductive isolation 84 and genetic distance. These phylogeographic studies highlight the high and likely under-sampled 85 diversity of copepods, as well as the complex histories of divergence and biogeography that 86 shape their current genetic (reproductive) interactions. Despite greater appreciation of the extent 87 of species diversity among copepods, the ecological and evolutionary drivers of this diversity 88 and how it varies geographically and across taxonomic groups remains poorly understood. 89 Cryptic diversity in Acartia tonsa 5 90 A particularly interesting example of cryptic speciation exists for the calanoid copepod 91 Acartia tonsa, a numerically dominant species that is found in many of the world coastal oceans 92 and estuaries (Razouls 1965) and is tolerant of a wide range of environments and stressors (e.g. 93 Brylinski 1981, Cervetto et al. 1999, Gonzalez 1974). Initial molecular work using the 94 mitochondrial 16S marker revealed four distinct genetic clades with !10% divergence across the 95 Northwest Atlantic, which led authors to conclude that little genetic exchange likely occurred 96 among these lineages (Caudill & Bucklin 2004). Subsequent sequencing of the mitochondrial 97 COI gene, nuclear ITS region, and 16S in other studies showed that three or more lineages 98 occurred throughout the range of the species in the Western Atlantic and Europe, with 99 phylogenetic structure on the scale of ~ 1000-2000 km (Chen &Hare 2008, 2011; Chen 2009, 100 Drillet et al. 2008a). The three lineages in the NW Atlantic sort by salinity, with a ‘fresh’ (F) 101 lineage found at salinities below ~10, a ‘saline’ (S) lineage found primarily from 15 - 25 salinity 102 and an ‘intermediate’ (X) lineage residing at salinities of 10-22 (Fig. 1; Chen & Hare 2008, Chen 103 & Hare 2011,
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