Coalescent‐based species delimitation in North American pinyon pines using low‐copy nuclear genes and plastomes

Abstract

Premise: Accurate species delimitation is essential for evolutionary biology, conservation, and biodiversity management. We studied species delimitation in North American pinyon pines, Pinus subsection Cembroides, a natural group with high levels of incomplete lineage sorting. Methods: We used coalescent-based methods and multivariate analyses of low-copy number nuclear genes and nearly complete high-copy number plastomes generated with the Hyb-Seq method. The three coalescent-based species delimitation methods evaluated were the Generalized Mixed Yule Coalescent (GMYC), Poisson Tree Process (PTP), and Trinomial Distribution of Triplets (Tr2). We also measured admixture in populations with possible introgression. Results: Our results show inconsistencies among GMYC, PTP, and Tr2. The singlelocus based GMYC analysis of plastid DNA recovered a higher number of species (up to 24 entities, including singleton lineages and clusters) than PTP and the multilocus coalescent approach. The PTP analysis identified 10 species whereas Tr2 recovered 13, which agreed closely with taxonomic treatments. Conclusions: We found that PTP and GMYC identified species with low levels of ILS and high morphological divergence (P. maximartinezii, P. pinceana, and P. rzedowskii). However, GMYC method oversplit species by identification of more divergent samples as singletons. Moreover, both PTP and GMYC were incapable of identifying some species that are readily identified morphologically. We suggest that the divergence times between lineages within North American pinyon pines are so disparate that GMYC results are unreliable. Results of the Tr2 method coincided well with previous delimitations based on morphology, DNA, geography, and secondary chemistry.

Sequential hybridization may have facilitated ecological transitions in the Southwestern pinyon pine syngameon

“…As P. 9fallax is of hybrid origin, we expect to see its chlorotype grouping with either P. edulis or P. californiarum depending on the pollen donor; however, as P. californiarum likely inherited its chloroplast from P. edulis, the three taxa shared similar chlorotypes, while P. quadrifolia and P. monophylla remained distinct. A similar pattern using plastid data was found by Montes et al (2022) in which P. edulis, P. 9fallax, and P. californiarum formed a monophyletic group together but individually had paraphyly, while P. quadrifolia and P. monophylla formed their own monophyletic groups. Oddly, P. 9fallax was observed to have an intermediate level of heterozygosity between its two parental species, an unexpected observation of hybrid taxa.…”

“…This novel hybridization event was not detected in other genetic studies (i.e. Montes et al, 2019Montes et al, , 2022 likely due to their lower sample sizes and taxonomically focused sampling design targeting 'type' individuals. However, the hybrid origin of P. 9fallax may explain their study's nuclear phylogenetic findings wherein P. 9fallax samples never formed a monophyletic group, but instead grouped with either P. edulis or P. californiarum (Montes et al, 2022).…”

“…Montes et al, 2019Montes et al, , 2022 likely due to their lower sample sizes and taxonomically focused sampling design targeting 'type' individuals. However, the hybrid origin of P. 9fallax may explain their study's nuclear phylogenetic findings wherein P. 9fallax samples never formed a monophyletic group, but instead grouped with either P. edulis or P. californiarum (Montes et al, 2022). As P. 9fallax is of hybrid origin, we expect to see its chlorotype grouping with either P. edulis or P. californiarum depending on the pollen donor; however, as P. californiarum likely inherited its chloroplast from P. edulis, the three taxa shared similar chlorotypes, while P. quadrifolia and P. monophylla remained distinct.…”

“…While hybridization between fallax-type and P. edulis has been proposed (Lanner & Phillips, 1992;LaHood, 1995), no genetic studies have found evidence of admixture between the two taxa (Duran et al, 2012;Montes et al, 2019) and Montes et al (2022) found no genetic differentiation between them, implying that the two are one taxon. Fallax-type typically has one needle per fascicle with two resin canals (Little, 1968;Cole et al, 2008), whereas P. edulis has two needles and two resin canals.…”

“…This investigation includes two additional taxa that may also participate in this pinyon pine syngameon: P. edulis and the taxonomically controversial fallax-type (Lanner, 1971(Lanner, , 1974aLanner & Hutchison, 1972). Pinus edulis and the hypothesized fallax-type form a monophyletic group with the other three syngameon participants (Montes et al, 2022) and partially overlap in distribution (Fig. 1).…”