Insights into the neutral and adaptive processes shaping the spatial distribution of genomic variation in the economically important Moroccan locust (Dociostaurus maroccanus).

María José González-Serna,Joaquín Ortego,Pedro J Cordero

doi:10.1002/ece3.6165

Abstract

Understanding the processes that shape neutral and adaptive genomic variation is a fundamental step to determine the demographic and evolutionary dynamics of pest species. Here, we use genomic data obtained via restriction site‐associated DNA sequencing to investigate the genetic structure of Moroccan locust (Dociostaurus maroccanus) populations from the westernmost portion of the species distribution (Iberian Peninsula and Canary Islands), infer demographic trends, and determine the role of neutral versus selective processes in shaping spatial patterns of genomic variation in this pest species of great economic importance. Our analyses showed that Iberian populations are characterized by high gene flow, whereas the highly isolated Canarian populations have experienced strong genetic drift and loss of genetic diversity. Historical demographic reconstructions revealed that all populations have passed through a substantial genetic bottleneck around the last glacial maximum (~21 ka BP) followed by a sharp demographic expansion at the onset of the Holocene, indicating increased effective population sizes during warm periods as expected from the thermophilic nature of the species. Genome scans and environmental association analyses identified several loci putatively under selection, suggesting that local adaptation processes in certain populations might not be impeded by widespread gene flow. Finally, all analyses showed few differences between outbreak and nonoutbreak populations. Integrated pest management practices should consider high population connectivity and the potential importance of local adaptation processes on population persistence.

Highlights

| MATERIALS AND METHODSBetween May and July 2011–2016, we prospected adequate habitats for the Moroccan locust (Dociostaurus maroccanus) (i.e., grazed grasslands, natural sparse vegetation, arid or semidesert steppes, and abandoned agricultural fields; Latchininsky, 1998; Latchininsky, 2013) in the Iberian Peninsula and the Canary Islands
Our study shows for the first time that populations of the economically important Moroccan locust present a shallow genetic differentiation and little differences in past demography, putative signatures of selection, and contemporary levels of genetic diversity and structure between outbreak and nonoutbreak populations
Outbreaks of Moroccan locust are usually linked to considerable cattle densities and overgrazing (Latchininsky, 1998; Louveaux et al, 1996), and it has been suggested that their frequency might increase in the future favored by global warming (Aragón et al, 2013)

Summary

| MATERIALS AND METHODS

Between May and July 2011–2016, we prospected adequate habitats for the Moroccan locust (Dociostaurus maroccanus) (i.e., grazed grasslands, natural sparse vegetation, arid or semidesert steppes, and abandoned agricultural fields; Latchininsky, 1998; Latchininsky, 2013) in the Iberian Peninsula and the Canary Islands. We used Stairway plot (Liu & Fu, 2015) to reconstruct the demographic history of the studied populations, a novel model-flexible method based on the site frequency spectrum (SFS) that does not require whole-genome sequence data or reference genome information to infer changes in effective population size (Ne) over time These analyses were restricted to populations with eight genotyped individuals (see Figure 2 and Table 1), as the calculation of the SFS requires a downsampling procedure to remove missing data. Population genetic statistics (P, HO, HE, π, FIS) calculated in stacks for all positions (polymorphic and nonpolymorphic) are presented in FIGURE 3 Venn diagrams showing the overlap of number of loci identified as being putatively under selection by Arlequin (FDIST method) (red circles) and Bayescan (blue circles) and presenting environmental associations according to LFMM (yellow circles) for analyses based on (a) all populations and (b) restricted to populations from the Iberian Peninsula. Canarian populations showed a long period of stability in the past (200–100 ka BP) followed by a demographic bottleneck during the last glacial period (100–21 ka BP) and a subsequent expansion at the onset of the Holocene to reach contemporary effective population sizes of 220,000–350,000 diploid individuals (Figure 2c; Figure A7)

Findings

| DISCUSSION

| Conclusions and prospects