Admixture between Ancient Lineages, Selection, and the Formation of Sympatric Stickleback Species-Pairs

Abstract

Ecological speciation has become a popular model for the development and maintenance of reproductive isolation in closely related sympatric pairs of species or ecotypes. An implicit assumption has been that such pairs originate (possibly with gene flow) from a recent, genetically homogeneous ancestor. However, recent genomic data have revealed that currently sympatric taxa are often a result of secondary contact between ancestrally allopatric lineages. This has sparked an interest in the importance of initial hybridization upon secondary contact, with genomic reanalysis of classic examples of ecological speciation often implicating admixture in speciation. We describe a novel occurrence of unusually well-developed reproductive isolation in a model system for ecological speciation: the three-spined stickleback (Gasterosteus aculeatus), breeding sympatrically in multiple lagoons on the Scottish island of North Uist. Using morphological data, targeted genotyping, and genome-wide single-nucleotide polymorphism data, we show that lagoon resident and anadromous ecotypes are strongly reproductively isolated with an estimated hybridization rate of only ∼1%. We use palaeoecological and genetic data to test three hypotheses to explain the existence of these species-pairs. Our results suggest that recent, purely ecological speciation from a genetically homogeneous ancestor is probably not solely responsible for the evolution of species-pairs. Instead, we reveal a complex colonization history with multiple ancestral lineages contributing to the genetic composition of species-pairs, alongside strong disruptive selection. Our results imply a role for admixture upon secondary contact and are consistent with the recent suggestion that the genomic underpinning of ecological speciation often has an older, allopatric origin.

Phenotypic and genotypic parallel evolution in parapatric ecotypes ofSenecio

“…To characterize the extent of phenotypic and genotypic parallelism within a system, it is necessary to rigorously demonstrate that populations adapting to similar environments (collectively referred to as an ecotype) have arisen multiple times independently. We refer the reader to our previous analyses of parallel evolution in Senecio lautus (Roda et al, 2013b;James et al, 2020) and to systems such as the marine snail, Littorina saxatilis (Quesada et al, 2007;Johannesson et al, 2010;Bierne et al, 2013;Butlin et al, 2014;Pérez-Pereira et al, 2017), and the threespine stickleback, Gasterosteus aculeatus (Colosimo et al, 2005;Chan et al, 2010;Dean et al, 2019;Marques et al, 2019) where one can find some of the strongest evidence for the independent origin of populations, and to the increasing number of potential cases of parallel evolution in plants (Foster et al, 2007;Ostevik et al, 2012;Trucchi et al, 2017;Cai et al, 2019;Konečná et al, 2019;Knotek et al, 2020).…”

Courtship behavior, nesting microhabitat, and assortative mating in sympatric stickleback species pairs

“…Courtship behavioral differences often play a key role in maintaining adaptive divergence in stickleback, and this has been particularly well studied in divergent benthic–limnetic (Foster, 1995; Foster et al, 2008; Shaw et al., 2007), lake–stream (Delcourt et al., 2008; Raeymaekers et al., 2010) and japan sea anadromous—pacific ocean anadromous ecotypes (Kitano et al., 2007). Lagoon stickleback have only recently been recognized as an ecotype in their own right (Dean et al., 2019; Ravinet et al., 2015), and so their courtship behavior has not previously been investigated. We showed that lagoon males performed fewer of many of the classic stickleback courtship behaviors than males of the other two ecotypes (or sometimes none).…”

“…Anadromous fish are much larger, more heavily armored and differ from resident ecotypes in body shape and various trophic morphological traits such as gill raker number, reflecting their more pelagic lifestyle (see Figure 1 for photographs of different ecotypes). Reproductive isolation in species pairs is strong despite low levels of gene flow (Dean et al., 2019), and there is likely strong selection against hybrids, many of which probably attempt to migrate to sea without the full suite of associated traits. Hybrid fish, for example, often exhibit an intermediate lateral plate phenotype (Dean et al., 2019), which would likely make them more vulnerable to predation.…”

“…Reproductive isolation in species pairs is strong despite low levels of gene flow (Dean et al., 2019), and there is likely strong selection against hybrids, many of which probably attempt to migrate to sea without the full suite of associated traits. Hybrid fish, for example, often exhibit an intermediate lateral plate phenotype (Dean et al., 2019), which would likely make them more vulnerable to predation. Assortative mating may be important for maintaining reproductive isolation in lagoon–anadromous species pairs but, to the best of our knowledge, has never previously been tested.…”

Habitat preference and diverse migration in threespine sticklebacks, Gasterosteus aculeatus and G. nipponicus

“…The fish are widely distributed in various aquatic environments such as freshwater, brackish water and seawater, and have been divided into an anadromous type and a freshwater resident (fluvial) type 1 . The freshwater type was found to have recolonized from anadromous populations after the last deglaciation approximately ~ 10,000-20,000 years ago [6][7][8][9][10][11][12][13][14][15] . Anadromous and freshwater resident stickleback populations are usually allopatric but are occasionally parapatric or sympatric 7,[16][17][18][19][20][21][22][23][24] .…”