Population genetics of the European rabbit along a rural-to-urban gradient

Madlen Ziege,Panagiotis Theodorou,Bruno Streit,Stefan Merker,Hannah Jüngling,Martin Plath,Hannes Lerp

doi:10.1038/s41598-020-57962-3

Abstract

The European rabbit (Oryctolagus cuniculus) is declining in large parts of Europe but populations in some German cities remained so far unaffected by this decline. The question arises of how urbanization affects patterns of population genetic variation and differentiation in German rabbit populations, as urban habitat fragmentation may result in altered meta-population dynamics. To address this question, we used microsatellite markers to genotype rabbit populations occurring along a rural-to-urban gradient in and around the city of Frankfurt, Germany. We found no effect of urbanization on allelic richness. However, the observed heterozygosity was significantly higher in urban than rural populations and also the inbreeding coefficients were lower, most likely reflecting the small population sizes and possibly on-going loss of genetic diversity in structurally impoverished rural areas. Global FST and G′ST-values suggest moderate but significant differentiation between populations. Multiple matrix regression with randomization ascribed this differentiation to isolation-by-environment rather than isolation-by-distance. Analyses of migration rates revealed asymmetrical gene flow, which was higher from rural into urban populations than vice versa and may again reflect intensified agricultural land-use practices in rural areas. We discuss that populations inhabiting urban areas will likely play an important role in the future distribution of European rabbits.

Highlights

As cities expand worldwide, urban areas will double in size, cover approximately 10% of Earth’s landmass, and host around 5 billion people by 20301
We explored the relationship between the urbanity index and rarefied allelic richness as well as inbreeding coefficients using linear mixed-effects models (LMM)
We found a significant relationship between the urbanity index and HO (GLMM; χ2 = 4.224, p = 0.039) and FIS (LMM, χ2 = 17.008, p < 0.001), and HO increased, while FIS decreased from rural over suburban towards urban populations (Table 1, Fig. 2)

Summary

Introduction

Urban areas will double in size, cover approximately 10% of Earth’s landmass, and host around 5 billion people by 20301. Increased urbanization does not reduce gene flow nor genetic diversity in the downy yellow viole (Viola pubescens)[19], orchid bees (Euglossa viridissima and E. dilemma)[20], the spotted salamander (Ambystoma maculatum)[21], the west coast ctenotus (Ctenotus fallens)[22], the ornate box turtle (Terrapene ornata)[23], the red-tailed bumblebee (Bombus lapidarius)[24] and the Eurasian tree sparrow (Passer montanus)[25] This is not surprising, as the effects of urbanization are likely dependent on the form and intensity of land use, the spatial scale of investigation, and especially ecological attributes of the studied taxonomic group (e.g. dispersal ability, reproductive biology, diet and historical demography). In a study of white-footed mouse populations in the New York City metropolitan area, Munshi-South et al.[13] used IBD and IBE modelling to demonstrate that urbanization (i.e., IBE) drives genetic differentiation to a greater extent than geographic distances (i.e., IBD)

Methods

Results

Conclusion