Abstract
A new homoploid hybrid lineage needs to establish a degree of reproductive isolation from its parent species if it is to persist as an independent entity, but the role hybridization plays in this process is known in only a handful of cases. The homoploid hybrid ragwort species, Senecio squalidus (Oxford ragwort), originated following the introduction of hybrid plants to the UK approximately 320 years ago. The source of the hybrid plants was from a naturally occurring hybrid zone between S. aethnensis and S. chrysanthemifolius on Mount Etna, Sicily. Previous studies of the parent species found evidence for multiple incompatibility loci causing transmission ratio distortion of genetic markers in their hybrid progeny. This study closes the hybridization triangle by reporting a genetic mapping analysis of the remaining two paired cross combinations between S. squalidus and its parents. Genetic maps produced from F2 mapping families were generally collinear but with half of the linkage groups showing evidence of genomic reorganization between genetic maps. The new maps produced from crosses between S. squalidus and each parent showed multiple incompatibility loci distributed across the genome, some of which co-locate with previously reported incompatibility loci between the parents. These findings suggest that this young homoploid hybrid species has inherited a unique combination of genomic rearrangements and incompatibilities from its parents that contribute to its reproductive isolation.
Highlights
Hybridization is an important contributor to biodiversity and speciation with approximately 25% of all plant species and 10% of all animal species estimated to have experienced hybridization during their evolution (Mallet 2005; Baack and Reiseberg 2006)
The Senecio aethnensis and S. chrysanthemifolius F0 parental individuals were originally sampled as seed from populations VB and C1 on Mount t Etna as described in James and Abbott (2005), while the S. squalidus F0 individual was ip sampled as seed from the Oxford (Ox), UK, population as described in Hiscock (2000). cr Reciprocal controlled crosses were performed between parental individuals by gently s brushing together open flower heads and excluding illegitimate pollen transfer with u pollination bags before and after pollination as described in Hiscock (2000) to produce F1 n families where the maternal and paternal species of each individual were known
Reproductive te isolation of S. squalidus from its parents is primarily dependent on ecogeographic isolation, p with some isolating effects possibly resulting from genetic drift or selection during its origin e and establishment in the UK (James and Abbott 2005; Abbott et al 2009; Ross, 2010; c Brennan et al 2012), our results indicate that inherited genetic incompatibilities Ac contribute to the reproductive isolation of this homoploid hybrid species
Summary
Hybridization is an important contributor to biodiversity and speciation with approximately 25% of all plant species and 10% of all animal species estimated to have experienced hybridization during their evolution (Mallet 2005; Baack and Reiseberg 2006). Hybridization is effective at generating a range of new trait combinations and transgressive trait expression that occasionally enable hybrids to exhibit higher fitness than parents in particular ecological contexts (Buerkle et al 2000; Lexer et al 2003; Schwarz et al 2005; Jiggins et al 2008; Stelkens and Seehausen 2009) Under these conditions, positive selection can promote the establishment and persistence of new homoploid hybrid species even in the presence of ongoing gene flow (Buerkle et al 2000). Recent genetic mapping studies using F2 families derived from crosses between S. aethnensis and S. chrysanthemifolius have characterized genetic incompatibilities in the form of transmission ratio distortion (TRD), breakdown of fitness at the F2 generation, and associations between transmission ratio distortion loci (TRDL) and quantitative traits (Chapman et al 2013; 2016; Brennan et al 2014; 2016) These characteristics of hybrid crosses function as genetic incompatibilities by increasing reproductive barriers between taxa (Hall and Willis 2005; Moyle and Graham 2006). We Ac discuss our findings in terms of their wider implications for understanding hybridization and homoploid hybrid speciation
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