Influence of historical land use and modern agricultural expansion on the spatial and ecological divergence of sugarcane borer, Diatraea saccharalis (Lepidoptera: Crambidae) in Brazil

Abstract

Human-mediated changes in landscapes can facilitate niche expansion and accelerate the adaptation of insect species. The interaction between the evolutionary history of the sugarcane borer, Diatraea saccharalis Fabricius, and historical and modern agricultural activity in Brazil shaped its spatial genetic structure, facilitating ecological divergence and incipient host shifting. Based on microsatellite data, STRUCTURE analyses identified two (K = 2) and three (K = 3) significant genetic clusters that corresponded to: (a) a strong signal of spatial genetic structure and, (b) a cryptic signal of host differentiation. We inferred that K = 2 reflects the footprint of agricultural activity, such as expansion of crop production (sugarcane and maize), unintentional dispersion of pests, and management practices. In contrast, K = 3 indicated incipient host differentiation between larvae collected from sugarcane or maize. Our estimates of population size changes indicated that a historical bottleneck was associated with a reduction of sugarcane production ≈200 years ago. However, a more recent population expansion was detected (>1950s), associated with agricultural expansion of large crop production into previously unfarmed land. Partial Mantel tests supported our hypothesis of incipient host adaptation, and identified isolation-by-environment (e.g., host plant) in São Paulo and Minas Gerais states, where sugarcane has been traditionally produced in Brazil. The impact of agricultural production on D. saccharalis may continue, as the current population structure may hinder the efficacy of refuge plants in delaying insect resistance evolution to Bt toxin.

Host plant or geographic barrier? Reproductive compatibility among Diatraea saccharalis populations from different host plant species and locations in Argentina

“…Incipient signals of this divergence among SCB populations collected on various host plants (sugarcane and maize) were already observed by Pavinato et al. (), highlighting the importance to know the impact of this divergence on the gene flow among populations of SCB to develop sustainable pest control methods.…”

“…(, ), and Pavinato et al. (). In accordance with these studies, our results demonstrated pre‐ and post‐zygotic incompatibility in combinations of SCB populations in association with different host plants and differences in geographical distance.…”

“…() and Pavinato et al. () in populations of SCB from Brazil and USA with molecular tools, is also present in populations from Argentina. This association could conduce to a process called ecological speciation due to genetical divergence of the populations even if they were in contact (Schluter, ; Nosil, ).…”

“…On the basis of the molecular (Joyce et al., ; Pavinato et al., ) and reproductive studies (Fogliata et al., ) we would expect to continue finding reproductive incompatibility among SCB populations isolated geographically. On the other hand, it is necessary to assess whether the insect–host plant association found by Joyce et al.…”

“…These studies show evidence of the existence of barriers to gene flow, as a result of host plant associations. This could lead to reproductive isolation among populations from different host plants driven by phenological, phytochemical, and/or morphological differences (Bush, ; Diehl & Bush, , ), generating a process of speciation and divergence among these populations (Joyce et al., ; Pavinato et al., ).…”