Evolutionary Lineages of Marine Snails Identified Using Molecular
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Molecular Phylogenetics and Evolution xxx (xxxx) xxx–xxx Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Evolutionary lineages of marine snails identified using molecular phylogenetics and geometric morphometric analysis of shells ⁎ Felix Vauxa, , Steven A. Trewicka, James S. Cramptonb,c, Bruce A. Marshalld, Alan G. Beub, Simon F.K. Hillsa, Mary Morgan-Richardsa a Ecology Group (PN624), Private Bag 11222, Massey University, Palmerston North 4442, New Zealand1 b GNS Science, PO Box 30-368, Lower Hutt, New Zealand c School of Geography, Environment & Earth Sciences, Victoria University of Wellington, P.O. Box 600, Wellington, New Zealand d Museum of New Zealand Te Papa Tongarewa, P.O. Box 467, Wellington, New Zealand ARTICLE INFO ABSTRACT Keywords: The relationship between morphology and inheritance is of perennial interest in evolutionary biology and pa- Evolutionary lineage laeontology. Using three marine snail genera Penion, Antarctoneptunea and Kelletia, we investigate whether Geometric morphometric systematics based on shell morphology accurately reflect evolutionary lineages indicated by molecular phylo- Neogastropoda genetics. Members of these gastropod genera have been a taxonomic challenge due to substantial variation in Phenotype shell morphology, conservative radular and soft tissue morphology, few known ecological differences, and Phylogenomic geographical overlap between numerous species. Sampling all sixteen putative taxa identified across the three Speciation genera, we infer mitochondrial and nuclear ribosomal DNA phylogenetic relationships within the group, and compare this to variation in adult shell shape and size. Results of phylogenetic analysis indicate that each genus is monophyletic, although the status of some phylogenetically derived and likely more recently evolved taxa within Penion is uncertain. The recently described species P. lineatus is supported by genetic evidence. Morphology, captured using geometric morphometric analysis, distinguishes the genera and matches the mo- lecular phylogeny, although using the same dataset, species and phylogenetic subclades are not identified with high accuracy. Overall, despite abundant variation, we find that shell morphology accurately reflects genus-level classification and the corresponding deep phylogenetic splits identified in this group of marine snails. 1. Introduction overwhelming majority of taxa that have ever lived (Marshall, 2017). However, a significant problem for evolutionary analysis is that mor- A persistent problem for evolutionary biology and palaeontology is phological variation does not necessarily concord with the splitting and whether morphology accurately reflects phylogenetic relationships in a divergence of evolutionary lineages (Bapst, 2013; Vaux et al., 2016). given set of organisms. Morphological traits are desirable for systematic Consequently, instances where morphological change is concordant study because they can be considered across the entire range of living with phylogeny provide the best opportunity to estimate rates of evo- systems from subcellular pathogens (e.g. Roberts and Compans, 1998; lution over long periods of time (Hunt, 2013), as well as speciation and Diaz-Avalos et al., 2005), to unicellular (e.g. Siefert and Fox, 1998) and changes in diversity. multicellular organisms (e.g. Niklas, 2000; Valentin et al., 2002; Hills Molluscan shells have the potential to provide information about et al., 2012; Dowle et al., 2015). Morphology can be considered at both the pattern and process of morphological evolution. Their cal- numerous levels, including nucleic acid and protein structure (e.g. careous shells frequently preserve in good condition, meaning that Ender and Schierwater, 2003; Sakamaki et al., 2015), gametes (e.g. marine molluscs have some of the best-preserved fossil records of all Landry et al., 2003), and body plans (e.g. Niklas, 2000; Valentin et al., animals (Wagner, 2001; Crampton et al., 2006). Many lineages are 2002), and it includes obvious traits, often likely to be under selection, consequently used to investigate speciation and models of evolutionary that are intuitive to observe and measure. Morphology is the pre- change (e.g. Michaux, 1989; Wagner, 2001; Monnet et al., 2011; Hills dominant evidence preserved in the fossil record, which is our only et al., 2012; Collins et al., 2016; Combosch and Giribet, 2016). Shell source of primary data for the majority of evolutionary time and the morphology can capture features of development and growth ⁎ Corresponding author. E-mail addresses: [email protected], [email protected] (F. Vaux). 1 evolves.massey.ac.nz. https://doi.org/10.1016/j.ympev.2018.06.009 Received 8 February 2018; Received in revised form 5 June 2018; Accepted 5 June 2018 1055-7903/ © 2018 Elsevier Inc. All rights reserved. Please cite this article as: Vaux, F., Molecular Phylogenetics and Evolution (2018), https://doi.org/10.1016/j.ympev.2018.06.009 F. Vaux et al. Molecular Phylogenetics and Evolution xxx (xxxx) xxx–xxx Fig. 1. Geographical distributions of extant Penion, Antarctoneptunea and Kelletia species, showing sympatry of many taxa. The range of each putative taxon is highlighted in a different colour and an example shell is shown at the same scale (animal included for P. cuvierianus jeakingsi). References for geographical dis- tributions are given in the text. (A) The distribution of Penion taxa in New Zealand waters. Scale bars shown 150 km for map and 5 cm for shell photos. (B) The distribution of Australian Penion species, Antarctoneptunea and Kelletia throughout the Pacific Ocean. Scale bar shows 5 cm for shell photos. (Thompson, 1942; Seilacher and Gunji, 1993), reflect habitat and niche and South Korea (Hayashi, 2005; Hwang et al., 2014), and southern adaptation (e.g. Seilacher and Gunji, 1993; Vermeij, 1995), and even California and Baja Mexico, respectively (Zacherl et al., 2003). Further indicate the morphology of non-preserved soft tissue (e.g. Runnegar fossil Kelletia species are recorded from both regions as well as Ecuador and Bentley, 1983). However, instead of genetic difference, variation in (e.g. Anderson, 1910; Arnold, 1910; Addicott, 1970, Ozaki, 1954; shell morphology can also represent convergent evolution (e.g. Serb Olsson, 1964). One species of Antarctoneptunea is found in New Zealand et al., 2011), phenotypic plasticity in response to environmental var- waters (Dell, 1995; Vaux et al., 2017a) and another occurs off Antarc- iation (e.g. Palmer, 1990; Trussell, 2000, Hollander et al., 2006; tica (Dell, 1972, Fig. 1). The high taxonomic diversity of Penion in New Gemmell, 2017), or sexual dimorphism (e.g. Kurata and Kikuchi, 2000; Zealand corresponds with a high level of endemism for other marine Avaca et al., 2013). snails (Powell, 1979, Spencer et al., 2009, 2017), which is likely driven In this study we investigate whether variation in shell morphology is partially by the geographical remoteness of the region (Vaux et al., concordant with phylogenetic relationships among three closely related 2017a). gastropod genera: Penion P. Fischer, 1884, Antarctoneptunea Dell, 1972 Ecological and behavioural data that might aid the distinction of and Kelletia Bayle, 1884 (Neogastropoda, Buccinoidea). All three genera Penion, Antarctoneptunea and Kelletia species are scarce. All species are contain medium to large, benthic marine snails that exhibit consider- predator-scavengers (Rosenthal, 1971; Harasewych, 1998), and most able taxonomic and morphological diversity (Fig. 1). Molecular evi- occur on soft sediment basins in mid-shelf to bathyal depths dence supports a close relationship between these three genera (50–2000 m, Dell, 1956; Powell, 1979), although Kelletia and some (Hayashi, 2005; Vaux et al., 2017a), which was predicted by shell Penion species occur on rocky coastal substrates in shallow water morphology (Dell, 1972; Ponder, 1973). As with many other bucci- (0–50 m, Powell, 1979; Vendetti, 2009; Willan et al., 2010; Hwang noideans (e.g. Willan, 1978; Kantor, 2003; Walker et al., 2008), soft et al., 2013). All three genera have dioecious sexes (Rosenthal, 1970; part radular and opercular morphology is too conservative to distin- Ponder, 1973). There is a size difference in mating pairs of K. kelletii guish most taxa reliably (e.g. Dell, 1956; Ponder, 1973). Based on (Forbes, 1850) (Rosenthal, 1970), but there is no evidence for sec- traditional morphological measurements, adult (teleoconch) and larval ondary sexual dimorphism in the shell shape and size of P. chathamensis (protoconch) shells vary significantly within and between putative (Powell, 1938) (Vaux et al., 2017b). Despite apparent variation, there is species (e.g. Ponder, 1973; Powell, 1979; Beu and Maxwell, 1990). currently insufficient evidence for developmental traits to be used for Six extant species and one subspecies of Penion are currently re- the distinction of genera or species (Vaux et al., 2017a). Captive rearing cognised in New Zealand waters (Powell, 1979; Spencer et al., 2017; has demonstrated that the larvae of K. kelletii undergo indirect devel- Marshall et al., 2018), and a further two species are endemic to south- opment with facultative planktotrophy, potentially permitting long- eastern Australia (Ponder, 1973, Fig. 1). There is also a rich fossil re- distance dispersal (Vendetti, 2009). However, estimates regarding the cord for Penion in the South Pacific (e.g. Ponder, 1973; Beu and development