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