Geography, climate and shifts in host plants distribution explain the genomic variation in the cactus moth

Abstract

Landscape heterogeneity and the host plant use are factors suggested to play determinant roles in shaping the evolutionary history of herbivorous insects. However, the role of the reconfiguration of host plants distributions linked to Quaternary climate oscillations as drivers of contemporary population genetic structure is still poorly understood. Here, we formally examine the relative contribution of such factors on intraspecific diversification using the South American cactus moth, Cactoblastis cactorum, an herbivore insect specialized in the use of cacti as host plants. We assessed genomic variation using genome-wide SNPs and mitochondrial data in populations sampled across a broad geographical gradient where moths feed on different cactus species. We integrated demographic simulations and ecological niche modeling into a landscape genomics framework, to test alternative hypotheses of past and current population connectivity for both C. cactorum and its host plants. Regions exhibiting higher genomic diversity were evaluated for congruence with areas where suitable climatic conditions remained stable through time. Our results revealed that past spatial configuration of suitable habitat conditions and shifts of host plants distributions are the factors that better explain the intraspecific diversification. Genomic data also supported the hypothesis that areas of long-term habitat stability served as refugia for C. cactorum, enabling the maintenance of high levels of genetic diversity over time. Overall, our study highlights the importance of integrating inter-specific interactions and their spatio-temporal dynamics to better understand the relative importance of abiotic and biotic factors driving the diversification processes in herbivorous insects with broad geographical and restricted host ranges.

Climatic and soil characteristics account for the genetic structure of the invasive cactus moth Cactoblastis cactorum, in its native range in Argentina

“…Ecological niche modelling using bioclimatic variables indicated that environmental suitability increases since the last glacial maximum (ca. 21 ky) from the west to the east, north and south of the present distribution ( Poveda-Martínez et al, 2023 ). During the Spanish settlement in South America, five centuries ago, O. ficus-indica was introduced and likely colonized by C. cactorum since then ( Ervin, 2012 ).…”

“…This methodological approach is essential to test more realistic hypotheses of gene flow (Isolation by Environment, IBE) ( Orsini et al, 2013 ; Sexton, Hangartner & Hoffmann, 2014 ). However, to our knowledge, there have been few attempts to identify environmental barriers to gene flow of invasive species in their native range ( Sherpa et al, 2019 ; Acevedo-Limón et al, 2020 ; Poveda-Martínez et al, 2023 ). This kind of evidence is essential for population management as input for invasion dynamic modeling to predict the expansion range in non-native regions ( Brown et al, 2016 ; Aguirre-Liguori, Ramírez-Barahona & Gaut, 2021 ; Pilowsky et al, 2022 ).…”

“…Although some degree of preference to oviposit on the exotic O. ficus-indica rather than on other native species was recorded, C. cactorum behave as a generalist with little host preference ( Varone et al, 2014 ). Recent analyses using genome wide SNPs and niche modelling data indicated that past climatic changes during the Quaternary and shifts in host use conditioned the actual distribution of genetic variation of C. cactorum in Argentina ( Poveda-Martínez et al, 2023 ). Ecological niche modelling using bioclimatic variables indicated that environmental suitability increases since the last glacial maximum (ca.…”

“…During the Spanish settlement in South America, five centuries ago, O. ficus-indica was introduced and likely colonized by C. cactorum since then ( Ervin, 2012 ). The genetic structure of C. cactorum estimated across seven native hosts species suggest no evidence that the introduction of O. ficus-indica in the native range and the subsequent human-commercial dispersal have promoted contemporary admixture between distant populations ( Poveda-Martínez et al, 2023 ). Within Argentina, O. ficus-indica occupies a larger area and a wider environmental range than any of the other native Opuntia species ( Varone et al, 2014 ), representing a suitable system to examine possible contemporary environmental effects on genetic variation and structure without strong historical effects nested within native hosts distribution ( e.g ., Poveda-Martínez et al, 2023 ).…”

“…The genetic structure of C. cactorum estimated across seven native hosts species suggest no evidence that the introduction of O. ficus-indica in the native range and the subsequent human-commercial dispersal have promoted contemporary admixture between distant populations ( Poveda-Martínez et al, 2023 ). Within Argentina, O. ficus-indica occupies a larger area and a wider environmental range than any of the other native Opuntia species ( Varone et al, 2014 ), representing a suitable system to examine possible contemporary environmental effects on genetic variation and structure without strong historical effects nested within native hosts distribution ( e.g ., Poveda-Martínez et al, 2023 ). To control these sources of variation and to explore the contemporary environmental factors that affect the genetic structure of the species, in the present study, species-specific nuclear microsatellites were used to characterize the geographic pattern of genetic variation in C. cactorum associated with the distribution of O. ficus-indica .…”