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University of Copenhagen Evolutionary diversification in the marine realm A global case study with marine mammals Holt, Ben G.; Marx, Felix G.; Fritz, Susanne A.; Lessard, Jean Philippe; Rahbek, Carsten Published in: Frontiers of Biogeography DOI: 10.21425/F5FBG45184 Publication date: 2020 Document version Publisher's PDF, also known as Version of record Document license: CC BY Citation for published version (APA): Holt, B. G., Marx, F. G., Fritz, S. A., Lessard, J. P., & Rahbek, C. (2020). Evolutionary diversification in the marine realm: A global case study with marine mammals. Frontiers of Biogeography, 12(3), 1-14. https://doi.org/10.21425/F5FBG45184 Download date: 26. sep.. 2021 UC Merced Frontiers of Biogeography Title Evolutionary diversification in the marine realm: a global case study with marine mammals Permalink https://escholarship.org/uc/item/99s5x80m Journal Frontiers of Biogeography, 12(3) Authors Holt, Ben G. Marx, Felix G. Fritz, Susanne A. et al. Publication Date 2020 DOI 10.21425/F5FBG45184 Supplemental Material https://escholarship.org/uc/item/99s5x80m#supplemental License https://creativecommons.org/licenses/by/4.0/ 4.0 Peer reviewed eScholarship.org Powered by the California Digital Library University of California a Frontiers of Biogeography 2020, 12.3, e45184 Frontiers of Biogeography RESEARCH ARTICLE the scientific journal of the International Biogeography Society Evolutionary diversification in the marine realm: a global case study with marine mammals Ben G. Holt1,2* , Felix G. Marx3,4 , Susanne A. Fritz5,6 , Jean-Philippe Lessard7 , Carsten Rahbek1 1 Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Denmark; 2 Marine Biological Association of the UK, The Laboratory, Plymouth, UK; 3 Museum of New Zealand Te Papa Tongarewa, Wellington, New Zealand; 4 Department of Geology, University of Otago, Dunedin, New Zealand; 5 Senckenberg Biodiversity and Climate Research Centre (BiK-F), Frankfurt am Main, Germany; 6 Institute of Ecology, Evolution and Diversity, Goethe University, Frankfurt am Main, Germany; 7 Department of Biology, Concordia University, Montreal, Canada * Corresponding author: Ben G. Holt, [email protected] Abstract Highlights Speciation is thought to be predominantly driven by the • Marine mammals are an excellent case study for the geographical separation of populations of the ancestral role of geographically-driven diversification within species. Yet, in the marine realm, there is substantial open environments. biological diversity despite a lack of pronounced geographical barriers. Here, we investigate this paradox by considering • Evidence for geographically-driven speciation in the biogeography of marine mammals: cetaceans (whales cetaceans and pinnipeds is limited, albeit with some and dolphins) and pinnipeds (seals and sea lions). We test notable exceptions. for associations between past evolutionary diversification and current geographical distributions, after accounting for • Whereas cetaceans show a trend from ancient the potential effects of current environmental conditions. geographical dispersion towards more recent In general, cetacean lineages are widely dispersed and geographically-driven diversification, the opposite show few signs of geographically driven speciation, albeit is true of pinnipeds. with some notable exceptions. Pinnipeds, by contrast, show a more mixed pattern, with true seals (phocids) • Contemporary environmental factors play an important tending to be dispersed, whereas eared seals (otariids) role, with deep lineages among both groups clustering are more geographically clustered. Both cetaceans and within specific environmental conditions. pinnipeds show strong evidence for environmental • Environmental structuring may either be a consequence clustering of their phylogenetic lineages in relation to of environmentally-driven speciation, or, alternatively, factors such as sea temperature, the extent of sea ice, and may indicate that post-speciation range shifts have nitrate concentrations. Overall, current marine mammal biogeography is not indicative of geographical speciation largely erased signatures of geographically-driven mechanisms, with environmental factors being more diversification in marine mammals. important determinants of current taxonomic distributions. However, geographical isolation appears to have played a role in some important taxa, with evidence from the fossil record showing good support for these cases. Keywords: barriers, biogeography, dispersal, ecology, evolution, oceanic, phylo-betadiversity, phylogenetic diversity Introduction Assessing the importance of geographical isolation as a driver of speciation is often challenging. The vast “Since the ecology of marine organisms is fundamentally open expanse of the marine realm is a classic example different from that of such typical land animals as (Palumbi 1992). Compared to terrestrial environments, mammals, birds, land snails, and butterflies, one might high population connectivity within marine systems expect modes of speciation in the oceans that differ is thought to limit geographical separation, reducing completely from the typical geographic speciation of land opportunities for allopatric divergence (Palumbi 1992, animals.” (Mayr 1954) Bierne et al. 2003). Nevertheless, life in the oceans is e-ISSN: 1948-6596 https://escholarship.org/uc/fb doi:10.21425/F5FBG45184 © the authors, CC-BY 4.0 license 1 Holt et al. Marine mammal geographical diversification notably diverse, creating what has been coined the Data sources “marine speciation paradox” (Bierne et al. 2003). Some Comprehensive species-level phylogenies were studies have highlighted the role of ecological factors obtained from Higdon et al. (2007) and McGowen et al. in driving marine diversification (e.g., Momigliano et al. (2009). For Cetacea, several alternative phylogenies 2017). Beyond specific case studies, however, the were available (e.g., Steeman et al. 2009, Slater et al. extent to which geography drives speciation in the 2010). Of these, we selected McGowen et al. (2009) marine realm currently remains unclear. because of its comprehensive taxon sampling. Tests for the role of geographical isolation within Neophocaena asiaeorientalis, Orcaella heinsohni, open environments are confounded by post-speciation, Sousa teuszii, and Zalophus wollebaeki were manually environmentally-driven range shifts. Such distributional added to the phylogenies as sister species to their changes could erase speciation-related geographical congeners. Freshwater and landlocked species, patterns (Losos and Glor 2003); given that including the cetaceans Inia geoffrensis, Lipotes diversification typically occurs across hundreds of vexillifer, Platanista spp. and Sotalia fluviatilis, and thousands to millions of years (Hedges et al. 2015), the pinnipeds Pusa caspica and P. sibirica, were whereas environmental change can be far more removed. The final dataset comprised 82 cetacean rapid (Petit et al. 1999). As a result, assessments and 31 pinniped species. of geographically-driven diversification have been Global distributional data were based on the IUCN “frustratingly inconclusive” (Fitzpatrick et al. 2009). Red List of Threatened Species™ (IUCN 2016) and To avoid this pitfall, environmental variability needs to matched to the species list provided by the Society for be explicitly considered when assessing biogeographical Marine Mammalogy (2016). Species not recognised on this list were excluded. Species distributions can evidence for the geography of speciation. also be derived from computer models based on Here, we use a combination of current species environmental data. We avoided these data sources and distributions and phylogenetic data to test for instead relied on expert-derived range maps to avoid allopatric diversification in the two major groups of analytical circularity, as we included environmental marine mammals – cetaceans and pinnipeds – after data in our subsequent analyses (see ‘Environmental first accounting for environmental variation. Marine distance’ below). mammals are an excellent case study, owing to We amended our distributional data according to the existence of comprehensive phylogenies (e.g., the latest taxonomic information from the Society Steeman et al. 2009, Higdon et al. 2007, McGowen et al. for Marine Mammalogy. Thus, the distribution of 2009), distributional data (IUCN 2016) and a relatively Arctocephalus townsendi, which is listed as a species abundant fossil record (Marx et al. 2016, Berta et al. by the IUCN but as a subspecies of A. philippii by the 2018). In addition, cetaceans and pinnipeds provide Society for Marine Mammalogy, was added to that a useful comparison because of their fundamentally of A. philippii. Similarly, the distribution ofDelphinus different reproductive strategies, with the former capensis was added to that of D. delphis. being fully aquatic, while the latter must return to Distributional data were mapped and divided into land or ice to breed. grid cells based on an equal-area world grid in Behrmann projection, with cells equalling 148,953 km2 and Both allopatric divergence (Steeman et al. 2009) o and adaptive radiation (Slater et al. 2010, Marx and approximately equivalent to 4 latitude and longitude. Uhen 2010) have been proposed as primary drivers of This grid cell size is a compromise between data resolution and computational requirements and is extant cetacean diversity. Pinniped diversification is suitable for testing global
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