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Speciation with Gene Flow in Marine Systems

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Speciation with Gene Flow in Marine Systems Contributions to Zoology 88 (2019) 133-172 CTOZ brill.com/ctoz Speciation with gene flow in marine systems Gerrit Potkamp Department of Taxonomy & Systematics, Naturalis Biodiversity Center, PO Box 9517, 2300 RA Leiden, The Netherlands GELIFES – Groningen Institute for Evolutionary Life Sciences, Faculty of Science and Engineering, Groningen University, Nijenborgh 7, 9747 AG Groningen, The Netherlands Charles H.J.M. Fransen Department of Taxonomy & Systematics, Naturalis Biodiversity Center, PO Box 9517, 2300 RA Leiden, The Netherlands [email protected] Abstract Over the last century, a large body of literature emerged on mechanisms driving speciation. Most of the research into these questions focussed on terrestrial systems, while research in marine systems lagged behind. Here, we review the population genetic mechanisms and geographic context of 33 potential cases of speciation with gene flow in the marine realm, using six criteria inferred from theoretical models of speciation. Speciation with gene flow occurs in a wide range of marine taxa. Single traits, which induce assortative mating and are subjected to disruptive selection, such as differences in host-associations in invertebrates or colour pattern in tropical fish, are potentially responsible for a decrease in gene flow and may be driving divergence in the majority of cases. However, much remains unknown, and with the current knowledge, the frequency of ecological speciation with gene flow in marine systems re- mains difficult to estimate. Standardized, generally applicable statistical methods, explicitly testing dif- ferent hypotheses of speciation, are, going forward, required to confidently infer speciation with gene flow. Keywords assortative mating – disruptive selection – ecological speciation – magic trait – marine speciation – speciation with gene flow © potkamp & fransen, 2019 | doi:10.1163/18759866-20191344 This is an open access article distributed under the terms of the prevailing cc-by license at the time of publication. Downloaded from Brill.com10/11/2021 04:06:08AM via free access 134 POTKAMP & FRANSEN 1 Introduction Most research so far has dealt with specia- tion in terrestrial systems, while research on Since the modern synthesis of biology, specia- evolutionary mechanisms and speciation in tion without gene flow has been accepted as the marine realm has been lagging behind the default mode of speciation. An extrinsic (Miglietta et al., 2011; Peijnenburg & Goetze, barrier splits a population and prevents gene 2013; Bowen et al., 2016). Based on a study on flow between subpopulations, while genetic tropical echinoids, Mayr (1954) concluded incompatibilities between populations ac- that speciation in marine systems did not cumulate through genetic drift and gradually differ from speciation in terrestrial systems. result in reproductive isolation (Mayr, 1942, However, geographic barriers are seemingly 1963). Whether reproductive isolation can less common in marine systems compared to arise without extrinsic barriers has long been terrestrial systems, and many organisms have a discussion in the field of evolutionary biolo- a large dispersal potential because of long gy. In the absence of, for example, geographic pelagic larval stages (Palumbi, 1992; Hellberg, barriers, interbreeding may impede diver- 1998; Kinlan & Gaines, 2003; Rocha et al., 2005, gence within a population, which was already 2007; Rocha & Bowen, 2008; Miglietta et al., recognized by Wagner (1868) in his critique on 2011; but see Chen & Hare, 2011; Peijnenburg & Darwin (1859). However, since the second half Goetze, 2013; Goetze et al., 2017). Despite the of the twentieth century, mathematical mod- lack of obvious geographic barriers, diversity els of speciation with gene flow driven by dis- in marine systems can be very high. The shal- ruptive selection emerged (Maynard Smith, low-waters of the tropical latitudes, for exam- 1966; Dickinson & Antonovics, 1973; Rice, 1984, ple, are amongst the biologically most diverse 1987; Johnson et al., 1996; Kawecki, 1996, 1997; ecosystems, in some cases rivalling the bio- Dieckmann & Doebeli, 1999; Kondrashov & diversity seen in tropical rain forests (Reaka- Kondrashov, 1999; Doebeli & Dieckmann, Kudla, 1997; Plaisance et al., 2011; Fisher et al., 2000; Gavrilets, 2004). Empirical examples of 2015). Some authors therefore hypothesised divergence in sympatry, driven by disruptive that speciation with gene flow plays a larger selection (i.e., divergent selection within a role in marine systems compared to terres- single, panmictic population; Rundle & Nosil, trial ecosystems (Miglietta et al., 2011; Bowen 2005), were reported as well (Bush, 1969; Feder et al., 2013). Here, we review potential cases et al., 1988; Rice & Salt, 1988). The paradigm of of speciation with gene flow in marine sys- speciation in isolation as the sole mechanism tems. We discuss and compare the potential of speciation slowly shifted towards a view mechanisms driving divergence with gene incorporating speciation with gene flow as a flow among different case studies. We further plausible alternative (Bolnick & Fitzpatrick, discuss gaps in the current state of knowledge 2007). Currently, it is accepted that speciation and suggest directions for future research on can occur in the presence of gene flow (e.g., speciation with gene flow in marine systems. Hey, 2006; Bolnick & Fitzpatrick, 2007; Nosil, 2008). Literature has mostly focused on the biogeographic patterns, e.g., by comparing 2 Mechanisms of speciation with the frequency of allopatric vs. sympatric spe- gene flow ciation. The focus has recently shifted towards the population genetic process (Fitzpatrick Mathematical models of speciation with gene et al., 2008, 2009), where we focus on here. flow mostly follow a similar pattern. Disruptive Downloaded from Brill.com10/11/2021 04:06:08AM via free access SPECIATION WITH GENE FLOW IN MARINE SYSTEMS 135 selection in an initially panmictic popula- fate of cases of incipient speciation is not tion results in non-random mating and re- known, studying systems at different stages productive isolation within that population of speciation could provide a better insight (Maynard Smith, 1966; Bolnick & Fitzpatrick, into the mechanisms playing a role during 2007). With disruptive selection being the the process of speciation (Butlin et al., 2008). driver of divergence, speciation with gene It is likely that some hybridisation will occur flow can in most cases be considered a spe- among closely related species. The threshold cial case of ecological speciation, as defined value of hybridisation, below which reproduc- by Schluter (2009). It should be noted though tive isolation is considered to be ‘complete’, is that ecological factors and selection are likely impossible to determine exactly. Determining to play a role in other mechanisms of specia- such a value will always be arbitrary, trying tion as well (Schilthuizen, 2000; Schilthuizen to classify the continuous scale of hybridisa- et al., 2006; Sobel et al., 2010). Disruptive se- tion, from panmixia to full reproductive iso- lection on its own is, however, not sufficient lation, into discrete categories. Additionally, to maintain reproductive isolation, as random data on hybridisation are often scarce in less mating will counteract the genetic diversifica- well-studied species, and therefore difficult tion and reproductive isolation between sub- to quantify and compare among species. This populations (Bolnick & Fitzpatrick, 2007). makes assessing this criterion problematic. Assortative mating, for example through mate However, the effect of this lack of data will selection or (sub-) habitat differentiation, is not affect the conclusions of this study, as the required. Recombination between the assort- next criteria are more relevant to the question ment trait and the selected trait would, how- of the frequency of ecological speciation with ever, prevent the evolution of reproductive gene flow. isolation through disruptive selection (Felsen- Secondly, the four requirements for specia- stein, 1981), which has been coined the ‘selec- tion with gene flow are assessed: tion–recombination antagonism’ by Rice 2. Is there (potential for) disruptive (1984). Selection should therefore either indi- selection? rectly, in linkage disequilibrium, or directly af- 3. Do populations mate assortatively in fect the assortment trait causing non-random sympatry? mating for the evolution of reproductive iso- 4. Is the selected trait linked to the assort- lation to occur (Kirkpatrick & Ravigné, 2002). ment trait? Besides evidence for (historical) gene flow 5. Is there evidence for gene flow between after the divergence between populations, populations at the time of divergence? evidence for disruptive selection, assortative These criteria are derived from mathemati- mating, and a link between the selected trait cal models of speciation with gene flow (e.g., and the assortment trait should be present in Maynard Smith, 1966; Kawecki, 1997; Doebeli the studied populations to infer speciation & Dieckmann, 2000). The second, third, and with gene flow. fourth criterion were also used by Rundle We will evaluate cases of potential (in- & Nosil (2005) in their review of ecological cipient) speciation with gene flow against six speciation. The fifth criterion, which directly criteria. First, to identify cases of incipient tests for the occurrence of gene flow during speciation we ask: divergence, was added to exclude cases where 1. Are populations
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