Molecular evidence and ecological niche modeling reveal an extensive hybrid zone among three Bursera species (section Bullockia)

Abstract

The genus Bursera, includes ~100 shrub and trees species in tropical dry forests with its center of diversification and endemism in Mexico. Morphologically intermediate individuals have commonly been observed in Mexican Bursera in areas where closely related species coexist. These individuals are assumed to result from interspecific hybridization, but no molecular evidence has supported their hybrid origins. This study aimed to investigate the existence of interspecific hybridization among three Mexican Bursera species (Bullockia section: B. cuneata, B. palmeri and B. bipinnata) from nine populations based on DNA sequences (three nuclear and four chloroplast regions) and ecological niche modeling for three past and two future scenario projections. Results from the only two polymorphic nuclear regions (PEPC, ETS) supported the hybrid origin of morphologically intermediate individuals and revealed that B. cuneata and B. bipinnata are the parental species that are genetically closer to the putative hybrids. Ecological niche modeling accurately predicted the occurrence of putative hybrid populations and showed a potential hybrid zone extending in a larger area (74,000 km2) than previously thought. Paleo-reconstructions showed a potential hybrid zone existing from the Last Glacial Maximum (~ 21 kya) that has increased since the late Holocene to the present. Future ecological niche projections show an increment of suitability of the potential hybrid zone for 2050 and 2070 relative to the present. Hybrid zone changes responded mostly to an increase in elevational ranges. Our study provides the first insight of an extensive hybrid zone among three Mexican Bursera species based on molecular data and ecological niche modeling.

Fig 1. Leaf characteristics of (A) Bursera bipinnata, (B) B. cuneata, (C) B. palmeri and (D) putative hybrids, and (E) map of sampling localities.

Numbers within circles represent the number of samples collected per each species and the putative hybrids per locality; color designations: B. bipinnata (green), B. cuneata (blue), B. palmeri (yellow), and putative hybrids (pink). Sampling localities: Aguascalientes AGS, Jalisco JAL, Churintzio CH, Zacapu ZA, Pátzcuaro PTZ, Tarímbaro TM, Acumbaro AC, Ciudad de Mexico CDMX, Oaxaca, OAX.

Fig 2. Neighbor-net tree (A) and median-joining haplotype networks for 202 phased sequences of the (B) ETS and (C) PEPC nuclear genes in Bursera bipinnata (green), B. cuneata (blue), B. palmeri (yellow), and putative hybrids (pink).

Size of nodes is proportional to the number of sequences per haplotype, dashed lines represent the number of mutational steps separating haplotypes, and black nodes represent unsampled haplotypes.

Fig 3. (A) BAPS barplot of the best-supported K = 7 clusters and (B) DAPC plot of haplotypes in Bursera bipinnata (Bp), B. cuneata (Bc), B. palmeri (Bm), and the putative hybrids (Bh).

The insets showed the proportion of variance explained by each of the two DA eigenvalues (DA 1 & 2 respectively) and the number of retained PCA eingenvalues.

Fig 4. Ecological niche projections of the overlap zone among Bursera bipinnata, B. cuneata, and B. palmeri at the present and past scenarios.

(A) Hybrid leaf sample, (B) present time, (C) late Holocene (LH, CCSM4), (D) late Holocene (LH MIROC), (E) Last Glacial Maximum (LGM, CCSM), (F) Last Glacial Maximum (LGM, MIROC) and (G) Last Interglacial (LIG). Red areas on the map indicate the predicted overlap niche zones, purple dots represent the occurrence of hybrid populations, numbers in km represent the total extension of the hybrid zone.

Fig 5. Ecological niche predictions of the overlap niche zone among Bursera bipinnata, B. cuneata, and B. palmeri for future climatic scenarios: (A) 2050 optimistic scenario (RCP 4.5, CCSM4), (B) 2050 optimistic scenario (RCP 4.5, MIROC), (C) 2050 pessimistic scenario (RCP 8.5, CCSM4), (D) 2050 pessimistic scenario (RCP 8.5, MIROC), (E) 2070 optimistic scenario (RCP 4.5, MIROC), (F) 2070 pessimistic scenario (RCP 8.5, CCSM4), (G) 2070 pessimistic scenario (RCP 8.5, CCSM4), (H) 2070 pessimistic scenario (RCP 8.5, MIROC).

Red areas on the map indicate the predicted overlap niche zones, purple dots represent the occurrence of hybrid populations, and numbers in km represent the total extension of the hybrid zone.