Geography, climate and changes in host plants distribution explain patterns of genomic variation within the cactus moth
Running head: Genomic variation of the cactus moth
Daniel Poveda-Martínez1,2*, Víctor Noguerales3, Laura Varone1, Stephen D. Hight4, Guillermo Logarzo1, Brent C. Emerson3, Esteban Hasson2.
1Fundación para el Estudio de Especies Invasivas (FuEDEI), Hurlingham, Argentina.
2Instituto de Ecología Genética y Evolución de Buenos Aires (IEGEBA-CONICET), Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires, Buenos Aires, Argentina.
3Island Ecology and Evolution Research Group, Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), San Cristóbal de La Laguna, Canary Islands, Spain.
4USDA-ARS, Insect Behavior and Biocontrol Research Unit (IBBRU), Tallahassee, Florida, USA.
*Corresponding author:danielpovedam@gmail.com(D.P.M).
Abstract
Landscape heterogeneity and the reconfiguration of host plant distributions as a consequence of Quaternary climate oscillations are suggested to play a determinant role in shaping the evolutionary history of herbivorous insects. The cactus moth, Cactoblastis cactorum , is a southern South American phytophagous insect specialized in the use of cacti as feeding and breeding resources. It can be found across broad latitudinal and longitudinal gradients feeding on diverse nativeOpuntia species as well as the exotic and cultivated speciesOpuntia ficus-indica . Using high-throughput sequence data for the nuclear genome and mitochondrial DNA sequencing, we investigated patterns of genomic variation of C. cactorum across its native distribution. We integrated a demographic modeling approach for inferring gene flow and divergence times between C. cactorumpopulations, within a landscape genomic framework, to test alternative spatially-explicit hypotheses of past and current population connectivity based on climatically suitable areas for the focal species and distributions of host plants. Regions currently exhibiting high genomic diversity were evaluated for congruence with areas where suitable climatic conditions remained stable from the last glacial maximum to the present. Results revealed significant population structure across the range of C. cactorum , that can be explained by the spatial configuration of persistently suitable environmental conditions and host plant ranges during interglacial and glacial periods. Moreover, genomic data supported a hypothesis of long-term habitat stability in the northern regions of the distribution that served as a refuge for C. cactorum , enabling the accumulation and maintenance of high levels of genetic diversity over time.
Key words : Cactus pest, Cactoblastis cactorum , ddRAD, landscape genomics, paleoclimate, Opuntia .
Introduction
The study of herbivorous insect pests and the spatio-ecological factors affecting their historical and contemporary population genetic structure is of interest for both evolutionary understanding and pest management. When such studies involve species distributed across environmental gradients, with multiple host species, they can also provide a window on the processes driving diversification and shaping gene flow dynamics in heterogeneous landscapes (Borer, Arrigo, Buerki, Naisbit & Alvarez, 2012; Laukkanen, Mutikainen, Muola & Leimu, 2014).
The use of alternative host plants is thought to be a strong determinant in the evolutionary history of phytophagous insects (Forbes et al., 2017; Funk, Nosil, & Etges, 2006), a factor which together with adaptation to differing environmental conditions can lead to ecological specialization and diversification (isolation by environment, IBE; Wang & Bradburd, 2014). Geography (isolation by distance, IBD; Slatkin, 1993) and the spatial distribution of suitable habitats (isolation by resistance, IBR; McRae, 2006; McRae & Beier, 2007) may also be determinants of population genetic differentiation across the landscape (Driscoe et al., 2019; Peterman, Connette, Semlitsch & Eggert, 2014; Vidal, Quinn, Stireman III, Tinghitella & Murphy, 2019). Additionally, changes in host plant distributions driven by climate oscillations throughout the Quaternary period may have an important role in shaping contemporary patterns of genetic variation in species with narrow feeding requirements (Noguerales, Cordero & Ortego, 2018).
Southern South America has a complex and ancient geological history in which orogenic processes, such as the uplift of the Andes, together with marine transgressions and biotic landscape changes caused by Quaternary climatic oscillations, have been hypothesized to shape intra and interspecific diversification in the region (Agrain, Domínguez, Carrara, Griotti & Roig‐Juñent, 2021; Hewitt, 2000; Ortiz-Jaureguizar & Cladera, 2006; Rodriguero, Lanteri, Guzmán, Carús Guedes & Confalonieri, 2016). These historical events have synergistically contributed to promote periods of both population isolation and subsequent secondary contact (Lavinia, Barreira, Campagna, Tubaro & Lijtmaer, 2019; Rocha et al., 2020). Evidence for evolutionary consequences of landscape changes promoted by Quaternary climatic dynamics is being increasingly documented in southern South America. The distributional shifts of open vegetation biomes, such as the Chacoan and Pampean domains, have been hypothesized to determine the diversification history of many faunal taxa intimately linked to these habitats (Rodriguero et al., 2016; Rosetti, Krohling & Remis, 2022; Turchetto-Zolet, Pinheiro, Salgueiro & Palma-Silva, 2013).
Among the southern South America invertebrate fauna, the cactus moth,Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), provides a suitable opportunity to investigate the aforementioned factors and their potential role in diversification within the region. Cactoblastis cactorum is a phytophagous moth native to southern South America. It can be found across wide latitudinal and longitudinal gradients, from the arid and semi-arid lands of northwestern and northeastern Chaco, the grasslands of the Pampa, through to the northern area of the Patagonian steppe (McFadyen, 1985; Morrone, 2014; Varone, Logarzo, Briano, Hight & Carpenter, 2014) (Figure 1). Across its broad distribution, C. cactorum exploits a broad spectrum of host species within the genusOpuntia (Cactaceae, Opuntioideae), including several native species such as O. quimilo K. Schum., O. megapotamicaArechav., O. bonaerensis Speg., O. elata Link & Otto ex Salm-Dyck, O. rioplatense Font, O. anacantha Speg. andO. penicilligera Speg. and the exotic and commercially cultivatedO. ficus-indica (L.) Miller (Varone et al., 2012, 2014).
The affinity of C. cactorum for species of Opuntia(prickly pear cactus) has encouraged its use as a biological control agent since 1925, particularly during the successful programs against alien Opuntia species in Australia and South Africa (Julien & Griffiths, 1998). Despite the substantial success in controlling invasive cacti in Australia, the deliberate introduction of C. cactorum as a biological control agent into the Caribbean (Simmonds & Bennett 1966) resulted in threats to both cactus diversity as well as the prickly pear fruit industry in the Caribbean, and more recently in North America (Hight & Carpenter, 2009). In its native range, C. cactorum also represents a serious threat to the regional prickly pear fruit production industry based on the Mexican species O. ficus-indica . The use of this species as a feeding and breeding resource represents a relatively recent expansion of host use byC. cactorum (Ervin, 2012). Almost one third of O. ficus-indica crops are infested with C. cactorum in some regions of Argentina (Varone et al., 2014). Opuntia ficus-indica is considered a traditional crop in arid and semi-arid regions of Argentina, being part of family subsistence economies and also having a prominent role in the regional economy (Ochoa, Targa, Abdala & Leguizamón, 2007). While the prickly pear industry is mainly concentrated in central and northern Argentina, patches of O. ficus-indica can also be found in other parts of the country (Varone et al., 2014). This distribution has led to the suggestion that O. ficus-indica may promote the movement of C. cactorum among distant populations, through human activity
Previous studies have reported that populations of C. cactorumare not only genetically differentiated (Marsico et al., 2011), but that patterns of coloration of mature larvae and host plant use also vary across regions (Brooks, Ervin, Varone & Logarzo, 2012; McFadyen, 1985). However, only limited conclusions can be drawn from these studies, due to the following: (i) only a single mitochondrial genetic marker was used; (ii) sampling did not cover the entire species range; and (iii) the relative abundance of host species were not taken into account (Brooks et al., 2012; Marsico et al., 2011; McFadyen, 1985). More recently, an extensive survey evaluating host plant preferences across the broad range of C. cactorum concluded that patterns of host use reflect variation in host availability rather than female preference (Varone et al., 2014). In accordance with this finding, a recent study of C. cactorum and two closely related specialist species,Cactoblastis bucyrus Dyar and Cactoblastis doddi Heinrich, demonstrated that geography is more important than host species as a driver of genetic differentiation in C. cactorum , contrasting with the two specialist species for which intra-specific genetic differentiation is mainly determined by host species rather than geography (Poveda-Martinez et al., 2022). These findings are consistent with the idea that the use of alternative host species in generalist herbivores may not promote divergence, due to relatively low fitness variation across different host species (Vidal & Murphy, 2018; Vidal et al., 2019). However, additional work is needed for a complete understanding of the effects of spatiotemporal changes in landscape factors on the evolutionary history of C. cactorum in its native range (Varone et al., 2014; Poveda-Martínez et al., 2022).
In this study, we use high-throughput nuclear sequence data and Sanger sequence data for mitochondrial DNA to investigate the evolutionary history of the cactus moth, C. cactorum . We sample populations ofC. cactorum representatively across its broad geographic range and diversity of native and non-native host species. We combine inferences from phylogenomics and demographic modeling to uncover the tempo and mode of diversification among genetic groups, together with patterns of gene flow, population genetic structure and diversity. By integrating ecological niche modeling into a landscape genomic framework, we are able to test a comprehensive suite of competing scenarios of population isolation, specifically evaluating the hypotheses that (i) contemporary spatial patterns of population differentiation in C. cactorum can be explained by the geographic reconfiguring of suitable areas for the focal species and its host species, caused by Quaternary climate dynamics, and (ii) regions whereC. cactorum exhibits high genomic diversity, together with no evidence for genetic admixture, are those where suitable climatic conditions have remained stable from the last glacial maximum (LGM, ca. 21 ka) to the present-day. Finally, we also evaluated if the broadened distribution of O. ficus-indica resulting from its introduction and cultivation is facilitating contemporary gene flow among geographically distant populations, thus promoting genetic admixture within C. cactorum.
Methods