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Rapid and Predictable Evolution of Admixed Populations Between Two Drosophila Species Pairs

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Rapid and Predictable Evolution of Admixed Populations Between Two Drosophila Species Pairs Genetics: Early Online, published on November 25, 2019 as 10.1534/genetics.119.302685 Rapid and predictable evolution of admixed populations between two Drosophila species pairs Daniel R. Matute1, Aaron A. Comeault2, Eric Earley1, Antonio Serrato-Capuchina1, David Peede1, Anaïs Monroy-Eklund1, Wen Huang3,4, Corbin D. Jones1, Trudy F. C. Mackay3,5, and Jerry A. Coyne6 1 2 1Biology Department, University of North Carolina, Chapel Hill, N.C. USA 3 2School of Natural Sciences, Bangor University, UK 4 3Program in Genetics and Department of Biological Science, North Carolina State 5 University, Raleigh, NC 27695-7614 6 6Ecology and Evolution, University of Chicago, Chicago IL 60637 7 8 4Current Address: Department of Animal Science, Michigan State University, East 9 Lansing, MI 48842 10 5Current Address: Center for Human Genetics and Department of Genetics and 11 Biochemistry, Clemson University, Self Regional Hall, 114 Gregor Mendel Circle, 12 Greenwood, SC 29646 13 14 ¶ Correspondence: 15 Biology Department, University of North Carolina, Chapel Hill, North Carolina 16 250 Bell Tower Drive, Genome Sciences Building 17 Chapel Hill, NC 18 27510, USA RUNNING TITLE: Admixed Drosophila species KEYWORDS Hybridization, Introgression, Reproductive isolation, Speciation 19 Copyright 2019. 20 ABSTRACT 21 22 The consequences of hybridization are varied, ranging from the origin of new lineages, 23 introgression of some genes between species, to the extinction of one of the hybridizing 24 species. We generated replicate admixed populations between two pairs of sister 25 species of Drosophila: D. simulans and D. mauritiana; and D. yakuba and D. santomea. 26 Each pair consisted of a continental species and an island endemic. The admixed 27 populations were maintained by random mating in discrete generations for over 20 28 generations. We assessed morphological, behavioral, and fitness-related traits from 29 each replicate population periodically, and sequenced genomic DNA from the 30 populations at generation 20. For both pairs of species, species-specific traits and their 31 genomes regressed to those of the continental species. A few alleles from the island 32 species persisted, but they tended to be proportionally rare among all sites in the 33 genome and were rarely fixed within the populations. This paucity of alleles from the 34 island species was particularly pronounced on the X-chromosome. These results 35 indicate that nearly all foreign genes were quickly eliminated after hybridization and that 36 selection against the minor species genome might be similar across experimental 37 replicates. 38 39 INTRODUCTION 40 41 Hybridization between species in nature is more common than biologists suspected a 42 few decades ago. At least 10% of animal species can produce progeny when crossed 43 with individuals from a different species (Mallet 2005); the proportion seems to be 44 higher in plants (Stebbins 1950). The fitness outcomes of hybridization and admixture 45 are varied (Taylor and Larson 2019). Research on hybrid zones has revealed the extent 46 of gene exchange in nature and in some cases has identified alleles able to cross 47 species boundaries (reviewed in (Taylor et al. 2015; Moore 2015; Gompert et al. 2017). 48 Alleles that reside on sex chromosomes, however, are less likely to be transferred from 49 one species to another (Payseur et al. 2004, Macholan et al. 2007, Carneiro et al. 50 2010, 2014; Garrigan et al. 2012; Turissini and Matute 2017), while mtDNA seems to be 51 easily transferred across species boundaries (Bachtrog et al. 2006; Wallis et al. 2017). 52 A question that remains open is what outcome is expected when two species engage 53 not in sporadic gene exchange, but rather form an admixed population carrying many 54 genes from each of the two parental species. 55 Mass hybridization has three possible outcomes in terms of species persistence. 56 The first is that the two genomes could sort themselves into their initial parental 57 arrangements after hybridization; this will occur in instances where admixed genomes 58 are unfit and penalized by selection (Rosenblum et al. 2012). A second possibility is that 59 genomes can exist as a mosaic, with both genes from both parental species ancestries 60 persisting in a stable manner with roughly equivalent contributions from the parental 61 species (Schumer et al. 2016). A third possibility is that after admixture occurs, a few 62 alleles from one of the parental species can remain in a genetic background that 63 evolves back to one largely resembling a single parental species. In this last case, we 64 refer to the species that contributes the majority of alleles in the admixed genome as the 65 ‘major species’, and the one that contributes the minority of admixture as the ‘minor 66 species.’ 67 These scenarios have important implications for the way we understand genome 68 evolution and the general outcome of hybridization in nature. For example, under a 69 scenario where genomes do not tolerate introgression and behave as coadapted units, 70 we would expect admixed genotypes to be broadly selected against and the genetic 71 composition of hybrid populations to evolve towards that of a single parental species. 72 On the other hand, if the genomes of two species are largely compatible and can be 73 readily mixed (Mallet et al. 2016), potentially providing benefits to admixed individuals, 74 populations of hybrids would be expected to retain ancestry of both species and in 75 some instances even become isolated species themselves (i.e., hybrid speciation, 76 Mallet 2007, Chapman and Burke 2007, Mavarez and Linares 2008, Buerkle et al. 2000, 77 Schumer et al. 2013, Comeault and Matute 2018). These two outcomes are not 78 mutually exclusive, and in some cases large portions of the genome may be resistant to 79 admixture and introgression while other portions are free to move between species 80 boundaries, either as a result of being selectively neutral or selectively favored 81 (Schumer et al. 2014; Juric et al. 2016; Muirhead and Presgraves 2016). Both outcomes 82 have been observed. Hybridization can lead to purging of one of the genomes in which 83 the admixed individuals carry only a small proportion of one of the parental species 84 (Garrigan et al. 2012; Turissini and Matute 2017; Schrider et al. 2018), as well as to the 85 existence of stable and balanced mosaic genomes (Rieseberg et al. 2003; Fontaine et 86 al. 2015; Schumer et al. 2016). An aspect that remains largely unknown is whether 87 these outcomes are deterministic in repeated instances of hybridization. Evaluating this 88 hypothesis in nature is challenging because it requires identifying sets of species pairs 89 that show parallel instances of hybridization (e.g., parallel hybrid zones). 90 Alternatively, one can create fully admixed experimental populations in the lab, 91 where we can control the magnitude and nature of admixture, and directly observe the 92 outcome of hybridization between species. Using this experimental approach, we can 93 follow the evolution of phenotypes and genotypes after hybridization and determining if 94 certain parental traits or alleles are selectively favored or whether they can persist in a 95 fully admixed population. Additionally, if genomes persist as mosaics, this approach 96 may reveal whether independent instances of hybridization lead to the same genetic 97 mosaic in the genomes of admixed individuals. This approach has the advantage of 98 providing primary evidence of the amount of admixture that two genomes can tolerate 99 while also controlling for important features such as the timing of admixture and the 100 relative contribution of the parental species to the population of hybrids. Such an 101 experiment, therefore, has some advantages over studying admixture in natural 102 populations: aspects of demographic history can be controlled (and known) in an 103 experimental context. 104 Here we report the creation of replicate interspecific admixed populations using 105 two species pairs of Drosophila, followed by measuring the fate of multiple interspecific 106 trait differences in morphology and behavior as well as (via DNA sequencing) the 107 genetic composition of replicate populations of hybrids after 20 generations of 108 independent evolution. Each of the two species pairs was represented by a 109 continentally distributed species and a closely related island endemic. The island 110 parental species have experienced smaller long-term effective population sizes and 111 more “specialized” ecologies than the species distributed across the continent. The first 112 pair of species was D. simulans and D. mauritiana. D. simulans is widespread 113 throughout sub-Saharan Africa and has become an invasive species in much of the 114 world (Begun et al. 2007; Kofler et al. 2015). The species is presumed to have 115 originated either in East Africa or in Madagascar and populations from these regions 116 have the largest diversity of the whole range (Dean and Ballard 2004, Lachaise and 117 Silvain 2004, Kopp et al. 2006). D. mauritiana, on the other hand, is endemic to the 118 Indian Ocean island of Mauritius (David 1974). These two species are homosequential 119 in chromosome banding pattern: they do not differ in chromosome number or have 120 large-scale rearrangements that would impede recombination (Lemeunier and 121 Ashburner, 1976). The pair is thought to have diverged between 500 and 250 Kya 122 (Ks¾synonymous divergence¾ = 0.05) (Nunes et al. 2010; Garrigan et al. 2012). 123 Multiple barriers to gene flow separate the two species, including strong intraspecific 124 mating preferences and sterility of the hybrid males (Price et al. 2001; Lachaise et al. 125 2018). They also show multiple morphological and physiological differences (Coyne 126 1989; Laurie et al. 1997; Price et al. 2001). Even though no instances of natural 127 hybridization have been reported between these species, there is evidence of extensive 128 gene exchange in the recent past (Garrigan et al.
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