Our work delves into the diversity and genetic structure patterns and the demographic processes experienced during the invasion and spread of C. marmorata, as well as identifies the sources of origin of the invader lace bugs in Japan. Besides, we investigated potential future scenarios of its expansion under future climate conditions, considering the lace bug's high sensitivity to climatic variations, particularly temperature, which significantly impacts its successful development.
The COI sequences from the native populations showed high levels of haplotype diversity (Table 2), with 35 different haplotypes identified across the entire distribution. Surprisingly, there was no evidence of isolation by distance, or any pattern correlated with geographic location, which aligns with the overall low genetic structure observed among populations (Figs. 1 and 2; Table S1 and S2). This may be attributed to a substantial level of gene flow and population admixture, as indicated by the COI Structure analysis, where most populations align with the red and green clusters (see Fig. 1b) Interestingly, like it’s host plant the goldenrod, the lace bug populations displayed higher genetic structure values for organelle markers compared to nuclear markers (i.e., cp and mt), which may mirror differences in population size as delineated by each marker (Sakata et al. 2015). Notably, in its native range, the goldenrod exhibited a weak but significant association between genetic and geographic distance (Sakata et al., 2015), however, in the case of lace bugs, while certain populations exhibited relatively high genetic structure values when paired, no evidence of isolation by distance was detected. Furthermore, the demographic analysis conducted on native lace bug populations, suggests a recent selective sweep followed by an ongoing population expansion as suggested by the value of Tajima's D. This dynamic could potentially influence the current distribution of genetic diversity (Ortego et al. 2021; Parvizi et al. 2023; Webster et al. 2023), supported by the haplotype’s groups formed by hap1 and hap3 (Fig. 1a and b) and the overall low paired genetic structure (Table 3). Historical population declines have been observed in Northern Hemisphere insects, such as Harmonia axyridis, Coenonympha hero, and Nyctelia confuse. It has been proposed that the Last Glacial Maximum triggered a demographic collapse, subsequently followed by a population expansion, as indicated by genetic and demographic signatures (Li et al. 2020, 2023; Sherpa and Després 2021). Our genetic evidence is consistent with the findings of Sakata et al. (2015), as the cp markers for goldenrod suggest a recent post-glacial population expansion which has contributed to the current genetic structure patterns of the native lace bug populations.
Table 5
Analysis of molecular variance for SNP´s markers in Corythucha marmorata populations from USA and Japan. The proportions of genetic variation among countries and within and between populations are shown.
Source of variation
|
d.f.
|
Sum of squares
|
Variance components
|
Percentage of variation
|
Among Countries
|
1
|
32.337
|
0.89154
|
10.66
|
Among populations within Countries
|
4
|
40.953
|
0.32123
|
3.84
|
Within populations
|
52
|
371.658
|
7.14728
|
88.40
|
Total
|
57
|
444.948
|
8.36004
|
|
FST= 0.14; FSC=0.04; FCT=0.10664 |
The mitochondrial COI sequences exhibited different ancestry origins for the invasive populations. Although we found eight private haplotypes and significant genetic structure among countries, the genetic assignment exhibits the red cluster as the most frequent (Fig. 2), consistent with the Bayesian phylogeny (Fig. 1b). The most frequent haplotype in Japan (hap1; Fig. 1a) was also notably high in frequency among North American populations, further highlighting the interconnectedness revealed by our genetic analyses. Moreover, certain populations (i.e., TK, TY, KG, KC, SF, NAG, SAG) exhibit a genetic ancestry linked to the blue cluster present in the northernmost Canadian samples. This observation aligns with the Bayesian grouping, illustrating that most Japanese haplotypes cluster with exclusive Canadian haplotypes (i.e., hap35 and hap36; Fig. 1b). Additionally, our findings provide significant evidence of a sudden population contraction, as indicated by COI Tajima's D (Table 2). This contraction is consistent with the recent introduction of the species into Japan, further supported by the lower haplotype diversity observed in invasive populations compared to native ones.
Invasive species typically carry a limited portion of the genetic diversity found in their source populations. However, the variability of invader diaspores depends on both the quantity and frequency of colonizers (Parvizi et al., 2023; Smith et al., 2020; North et al., 2020). Our examination of single nucleotide polymorphisms (SNPs) in native lace bug populations unveiled moderate levels of genomic diversity, as evidenced by observed heterozygosity (Hₒ), expected heterozygosity (Hₑ), and nucleotide diversity (π) within the three native populations under investigation (Table 3).
Furthermore, we observed a low genetic differentiation among these native populations, aligning with the outcomes of the sNMF clustering analysis. These revealed distinct genetic ancestries, showing a pronounced separation between native and invasive populations, particularly at K = 2 and K = 3 (refer to Figs. 3 and 4). Notably, the northernmost population (LAK/ARK) exhibited contributions from all three genetic clusters. Moving southward, the green cluster became predominant in LMS/MIS, while the red cluster prevailed in the LFL/LFL2 population. However, LFL3/FL3 demonstrated admixture from all three genetic groups. In the case of K = 3, populations LC/CER and LS/SAG almost entirely belonged to the blue cluster, contrasting with its low frequency in the native northernmost population (LAK/ARK) and LFL3/LFL3 from the southern US (see Figs. 3 and 4). Similar patterns have been observed in invasive insects like Harmonia axyridis, native to East Asia (China, Japan, and Korea), which displayed high admixture levels from the USA and China in European standing populations (Li et al., 2020). Additionally, Halomorpha halys exhibited strong admixture patterns in invasive populations in the US and Europe originating from various East Asian sources (Parvizi et al., 2023).
Nevertheless, despite the observed low genetic structure among countries, the pairwise Fst analysis unequivocally reveals significant genetic differentiation among populations grouped into the blue and red clusters (Fig. 4; Table S2). This differentiation is evident in variations in allele frequencies rather than allelic identities, consistent with findings from Webster et al. (2023) and Parvizi et al. (2023). On a broader scale, the scarcity of private alleles in both mitochondrial (mt) and nuclear markers suggests that invader populations likely originated from a few independent sources (Sakata et al., 2015; Ortego et al., 2021; Parvizi et al., 2023; Li et al., 2023). The prevalence of a single genetic cluster for both markers could indicate robust novel selection pressures on genotypes, potentially influenced by the host plant (Sakata et al., 2015; Parvizi et al., 2023; Li et al., 2023). The widespread presence of tall goldenrod in Japan has been facilitated by the existence of railroad corridors, creating continuous habitats. This environment may contribute to increased genetic flow and admixture among lace bug populations, akin to observations in the Hypogeococcus pungens complex in standing invasive populations in Puerto Rico (Poveda-Martínez et al., 2022).
Invasive species often display a wide ecological range, characterized by a capacity to exploit varied resources. They may also exhibit distinct ecological strategies such as preferences for specific hosts, which can be significantly different from those of native source populations (Sherpa et al., 2021; Siddiqui et al., 2023). Despite reports of lace bugs exploiting various hosts both in their native and invaded ranges, Rizkawati and Tsukada (2020) noted significantly lower larval development rates in hosts such as sweet potato (Ipomoea batatas), blue daze (Evolvulus pilosus), and eggplant (Solanum melongena). This highlights the lace bug's specialization on goldenrod.
Furthermore, as reported by Sakata et al. (2017), lace bug density was higher in Japan compared to its native range. This could be attributed to the absence of herbivores competing in the native range, coupled with positive selection and genetic admixture (Sakata et al., 2015; 2017; Parvizi et al., 2023; Sherpa et al., 2021). The absence of competitors may have enabled the lace bug invaders to increase their effective population size, thereby coping with low genetic diversity and enhancing its capacity to acquiring local adaptations (Gozzi et al., 2020; Cuthbert et al., 2018; Webster et al., 2023; Siddiqui et al., 2023). However, the demographic Tajima´s D analysis for COI still showed signatures of a sudden population contraction which is in line with the prevalence of genetic affiliation in populations for both markers (Figs. 1 and 2), supporting the colonization from few native sources (Verhoeven et al. 2011; Chown et al. 2015; Sakata et al. 2015; Daly et al. 2023).
Despite the extensive presence of the tall goldenrod in high latitudes in Japan, the lace bug has not yet colonized its entire distribution (Sakata et al. 2014, 2016).