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Evidence from European Butterfly Sister Species

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Evidence from European Butterfly Sister Species bioRxiv preprint doi: https://doi.org/10.1101/2020.09.04.282962; this version posted November 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 The Pleistocene species pump past its prime: 2 evidence from European butterfly sister species 1 1 2 3 Sam Ebdon* , Dominik R. Laetsch , Leonardo Dapporto , 3 4 5 4 Alexander Hayward , Michael G. Ritchie , Vlad Dinc˘a , Roger 6 1 5 Vila , and Konrad Lohse 1 6 Institute of Evolutionary Biology, University of Edinburgh, 7 Edinburgh, EH9 3FL, UK 2 8 ZEN lab, Dipartimento di Biologia dell'Universit`adi Firenze, 9 Firenze, Italy 3 10 Centre for Ecology and Conservation, University of Exeter, 11 Penryn Campus, Cornwall, TR10 9FE, UK 4 12 Centre for Biological Diversity, School of Biology, University of St 13 Andrews, Fife KY16 9TH, UK 5 14 Ecology and Genetics Research Unit, University of Oulu, Oulu, 15 Finland 6 16 Institut de Biologia Evolutiva (CSIC - Universitat Pompeu 17 Fabra), Passeig Mar´ıtimde la Barceloneta 37, ESP-08003 18 Barcelona, Spain 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.04.282962; this version posted November 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 19 * correspondence to [email protected] 20 21 Abstract 22 The Pleistocene glacial cycles had a profound impact on the ranges and genetic 23 make-up of organisms. Whilst it is clear that the contact zones that have been 24 described for many sister taxa are secondary and have formed during the last 25 interglacial, it is unclear when the taxa involved began to diverge. Previous es- 26 timates based on small numbers of loci are unreliable given the stochasticity of 27 genetic drift and the contrasting effects of incomplete lineage sorting and gene 28 flow on gene divergence. Here we use genome-wide transcriptome data to esti- 29 mate divergence for 18 sister species pairs of European butterflies showing either 30 sympatric or contact zone distributions. We find that in most cases species di- 31 vergence predates the mid-Pleistocene transition or even the entire Pleistocene 32 period. We also show that although post divergence gene flow is restricted to 33 contact zone pairs, they are not systematically younger than sympatric pairs. 34 This suggests that contact zones are not limited to the embryonic stages of the 35 speciation process, but can involve notably old taxa. Finally, we show that 36 mitochondrial and nuclear divergence are only weakly correlated and mitochon- 37 drial divergence is higher for contact-zone pairs. This suggests a possible role of 38 selective sweeps affecting mitochondrial variation in maintaining contact zones. 39 Impact Summary 40 The influence of the Pleistocene glacial cycles on structuring species and genetic 41 diversity in temperate taxa has permeated biogeographic and phylogeographic 42 thinking for decades. Although phylogeographic studies have repeatedly claimed 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.04.282962; this version posted November 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 43 that the Pleistocene acted as a species pump, systematic tests of this idea based 44 on robust estimates of species divergence are lacking. Here we estimate diver- 45 gence times for all sister species pairs of European butterfly using genome-wide 46 transcriptome data. We find that most species pairs are substantially older 47 than the onset of Pleistocene glacial cycling. We also show that post divergence 48 gene flow is restricted to pairs that form contact-zones. However, in contrast to 49 expectations under a null model of allopatric speciation contract zone pairs are 50 not necessarily younger than sympatric pairs. 51 Introduction 52 Divergence in allopatry provides a simple null model of speciation (Mayr, 1947). 53 Following geographic isolation and given enough time, reproductive isolation 54 is inevitable as incompatibilities will eventually become fixed as a result of 55 genetic drift and/or selection (Bateson, 1909, Dobzhansky, 1937, Muller, 1942). 56 Taxa that evolved partial reproductive isolation in allopatry may come into 57 secondary contact as a result of range shifts and { depending on their degree 58 of reproductive isolation and niche overlap { either form a contact zone or 59 invade each other's range (Barton & Hewitt, 1985, Pigot & Tobias, 2013). If 60 allopatric divergence dominates speciation, then local alpha diversity for a given 61 clade cannot accrue until secondary sympatry is achieved (Weir & Price, 2011). 62 Thus the forces that facilitate or hamper secondary sympatry and the timescale 63 over which this occurs have profound consequences both for speciation and the 64 spatial distribution of species diversity. While modern ranges only provide a 65 snapshot of the dynamic history of range shifts, understanding the extent to 66 which current range overlap between closely related species can be explained 67 by their speciation history and vice versa has been at the core of speciation 68 research (Coyne & Orr, 2004). 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.04.282962; this version posted November 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 69 The glacial cycles of the Pleistocene had a profound effect on current diver- 70 sity of temperate ecosystems (Hewitt, 1996, 2001, Hofreiter & Stewart). Popu- 71 lations of temperate taxa in Europe were isolated in ice-free refugia around the 72 Mediterranean basin (Iberia, Italy, the Balkans and the larger Mediterranean 73 islands) as glaciers encroached. The observation that the geographic ranges of 74 many young taxa are restricted to individual glacial refugia in southern Europe 75 (Dennis et al., 1991, Hewitt, 1996, 1999, 2011) suggests that this repeated sepa- 76 ration into and expansion out of glacial refugia has played a major role in their 77 origin. The availability of allozyme and mitochondrial (mt) data in the 80s and 78 90s has spurred an abundance of case studies on intra- and interspecific diversity 79 of European taxa including detailed investigations of hybrid zones in taxa rang- 80 ing from fire-bellied toads (Kruuk et al., 1999), the house mouse (Boursot et al., 81 1996), grasshoppers (Barton, 1980, Butlin & Hewitt, 1985) to plants (Bacilieri 82 et al., 1996) and marine mussels (Skibinski & Beardmore, 1979). The pervad- 83 ing evidence from these studies is that genetic diversity within and in, many 84 cases, divergence between species is structured by refugia (Dapporto et al., 2019, 85 Hewitt, 1996, Schmitt, 2007a). 86 When was divergence between sister species initiated? 87 While it is clear that the hybrid zones we observe today are secondary contacts 88 that formed after the last glacial maximum and may have formed many times 89 over throughout the Pleistocene, it is far from clear when divergence between 90 the sister taxa involved was initiated. One possibility is that the Pleistocene 91 glacial cycles initiated species divergence directly by separating populations into 92 allopatric refugia (i.e. a 'species pump' sensu Haffer (1969)). Another possibil- 93 ity is that the initial divergence between sister species predates the Pleistocene, 94 and so, any build-up of reproductive isolation during the Pleistocene (e.g. via 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.04.282962; this version posted November 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 95 the fixation of intrinsic incompatibilities and/or reinforcement) occurred in pop- 96 ulations that were already partially diverged. If the Pleistocene species pump 97 hypothesis is correct, we would expect sister species divergence times to be 98 concentrated during or at the beginning of the mid-Pleistocene transition 0.8- 99 1.2 million years ago (MYA) which marks the onset of continent-wide glacial 100 cycling (Bishop et al., 2011). The idea that Pleistocene divergence acted as a 101 species pump was first proposed in the context of American faunas (Avise et al., 102 1998, Bernatchez & Wilson, 1998, Haffer, 1969), but has also dominated phy- 103 logeographic studies on European sister taxa (e.g. Habel et al., 2008, Hewitt, 104 2000, 1996, Schmitt, 2007b, Schoville et al., 2012). In contrast, other studies 105 including some of the early work on European contact zones (Barton & Hewitt, 106 1985, Butlin & Hewitt, 1985) conclude that the taxa involved in such secondary 107 contacts may substantially predate the Pleistocene (Abbott et al., 2000, Hewitt, 108 1996, Klicka & Zink, 1997, Spooner & Ritchie, 2006). Thus it remains unclear to 109 what extent divergence between sister taxa was initiated by 'Pleistocene species 110 pump' dynamics or has an older, deeper origin? 111 A corollary for the hypothesis of allopatric speciation in different refugia 112 is that range overlap is secondary. Since species can more easily invade each 113 others ranges once sufficient premating barriers and ecological differentiation 114 have developed, we would expect species pairs with overlapping ranges to be 115 older overall than those without range overlap, all else being equal (Coyne & Orr, 116 2004).
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