A Coevolutionary Arms Race Causes Ecological Speciation in Crossbills

Abstract

We examined three ecological factors potentially causing premating reproductive isolation to determine whether divergent selection as a result of coevolution between South Hills crossbills (Loxia curvirostra complex) and Rocky Mountain lodgepole pine (Pinus contorta latifolia) promotes ecological speciation. One factor was habitat isolation arising because of enhanced seed defenses of lodgepole pine in the South Hills. This caused the crossbill call types (morphologically and vocally differentiated forms) adapted to alternative resources to be rare. Another occurred when crossbills of other call types moved into the South Hills late in the breeding season and feeding conditions were deteriorating so that relatively few non-South Hills crossbills bred ("immigrant infecundity"). Finally, among those crossbills that bred, pairing was strongly assortative by call type (behavioral isolation). Total reproductive isolation between South Hills crossbills and the two other crossbills most common in the South Hills (call types 2 and 5) summed to .9975 and .9998, respectively, on a scale of 0 (no reproductive isolation) to 1 (complete reproductive isolation). These extremely high levels of reproductive isolation indicate that the divergent selection resulting from the coevolutionary arms race between crossbills and lodgepole pine is causing the South Hills crossbill to speciate.

Diversification and coevolution in brood pollination mutualisms: Windows into the role of biotic interactions in generating biological diversity

“…Even so, a number of studies have argued that hybridization between closely related sympatric figs mediated by shared pollinating fig wasps may be common (Jackson et al, 2008; Renoult et al, 2009; Cornille et al, 2011; Wang et al, 2016). The role of allopatry in speciation within pollination brood mutualisms is consistent with examples of potential coevolutionary speciation from other interactions (Parchman and Benkman, 2002; Hoso et al, 2010; Smith and Benkman, 2007; Schluter, 2010), in which geographic isolation was always implicated in diversification (Hembry et al, 2014). Continued examination of the role of geography and biotic selection in brood pollination mutualisms is crucial for understanding the mechanisms of speciation.…”

Assessing the Potential Contributions of Reduced Immigrant Viability and Fecundity to Reproductive Isolation

“…Because barriers that initiate divergence can be obscured as other barriers evolve, characterizing the evolution of RI early in speciation is difficult (Coyne and Orr 2004;Sobel et al 2010). Nevertheless, the few estimates of reduced immigrant fecundity from observational studies indicate that this barrier is fairly strong in nature (e.g., Smith and Benkman 2007;C. K. Porter, unpublished data), but more estimates from natural systems are needed to evaluate the generality of this pattern.…”

“…One, prezygotic isolating barriers appear much stronger than postzygotic isolating barriers early in speciation (Coyne and Orr 1989;Jiggins et al 2001;Ramsey et al 2003;Nosil et al 2005;Lowry et al 2008;Sobel and Streisfeld 2015). Two, isolating barriers closely tied to divergent natural selection (e.g., habitat isolation and immigrant inviability) are often particularly strong early in speciation (Ramsey et al 2003;Smith and Benkman 2007;Sobel 2014;Sobel and Streisfeld 2015;Ingley and Johnson 2016), supporting the hypothesis that adaptive divergence and speciation are fundamentally linked (Schluter 2000(Schluter , 2001(Schluter , 2009Schemske 2010;Sobel et al 2010;Nosil 2012).…”

“…While immigrant inviability has been estimated in multiple systems, the reduced ability or propensity of immigrants to reproduce has been identified as a form of reproductive isolation in only a single system (immigrant infecundity, per Smith and Benkman 2007), although the importance of reduced fecundity to reproductive isolation has long been appreciated (Coyne and Orr 2004;Harrison 2012). Because of the additional demands of reproduction beyond that required for maintenance, initial divergence might cause a greater depression in reproduction than in viability (Smith and Benkman 2007). Consistent with a greater sensitivity of reproduction than survival to variation in phenotype, fecundity selection is often stronger than viability selection (Kingsolver et al 2001;Hereford et al 2004) and is a stronger driver of local adaptation (Hereford 2009).…”

Ernst Mayr and the integration of geographic and ecological factors in speciation

“…, 1999), Acyrthosiphon pea aphids (Via, 1999; Hawthorne & Via, 2001), Neochlamisus leaf beetles (Funk, 1998; Egan, Nosil & Funk, 2008), Coregonus whitefish (Lu & Bernatchez, 1999; Campbell & Bernatchez, 2004), Gambusia fishes (Langerhans, Gifford & Joseph, 2007), Mimulus monkeyflowers (Macnair & Christie, 1983; Bradshaw & Schemske, 2003; Ramsey et al. , 2003), Loxia crossbills (Smith & Benkman, 2007), and Pundamilia cichlids (Maan et al. , 2006; Seehausen, 2008), amongst others (Rundle & Nosil, 2005).…”