High genetic variation and low gene flow among populations of Viscum verrucosum in semi-arid savanna, southwest Zimbabwe

Abstract

Despite the increasing recognition of the ecological role of mistletoes, little is known about their genetic diversity. In this regard, we assessed the genetic variation within and among populations of Viscum verrucosum using random amplified polymorphic DNA (RAPDs). Analysis of molecular variance (AMOVA) and phylogenetic analysis based on genetic distance matrices were used to partition variation within and among populations, and the relationship between geographical and genetic distance was established using a Mantel's test. Mean population genetic diversity was high (P = 77.19%, A = 1.58, h = 0.30, Hʹ = 0.44) relative to other outcrossing mistletoe species. Genetic differentiation among the populations was high (G_ST = 0.366), also with low gene flow (N_m = 0.433) among populations. The genetic distance was significantly correlated to geographic distance (r = −0.849, p = 0.002), consistent with isolation-by-distance model suggesting constrained genetic exchange between geographically distant populations. Consequently, most of the genetic variation was retained within (63%) than among (37%) populations. In conclusion, findings of this study suggest that isolation-by-distance coupled with low seed dispersal limit gene flow, and determine the high levels of genetic structure of V. verrucosum populations, while historically elevated rates of gene flow may explain the high genetic diversity detected in these populations.

Introduction

Mistletoes, through high transpiration rates, high litter nutrient concentrations, and extended periods of litterfall, act as ecosystem engineers and keystone species [1] altering host performance, soil moisture content, litterfall rates, and nutrient availability [2], [3], [4], which can ultimately influence local plant biomass, species composition and spatial distribution (e.g. grasses, [5], [6]. These changes to the understorey properties, together with additional mistletoe resources such as nutrient-rich foliage, flowers, fruits and nectar in infected host canopies, also alter the structure and function of animal assemblages (e.g. insects, [7], [8]; birds [9], [10]). However, despite the significant role played by parasitic plants in ecosystem structure and function, little is known about their genetic diversity.

In semi-arid savanna southwest Zimbabwe, woodlands are under increasing disturbance due to human activities such as deforestation and agricultural expansion. This has resulted in highly fragmented woodlands, with the remaining undisturbed woodlands occurring on private lands and conservation areas. In addition to reducing the size of woodland patches, fragmentation is expected to increase the geographical distance between woodland patches [11]. These changes are likely to affect gene flow between populations of both host trees and associated mistletoes, and consequently the genetic structure and diversity of mistletoes may be altered. Additionally, together with woodland fragmentation, the patchy distribution of mistletoes [12], [13] may further enhance isolation and increase genetic differentiation between populations [14]. However, studies on the genetic structure and diversity of mistletoe populations, and contributing factors are lacking in subtropical savanna.

Viscum is a genus of mistletoes represented by at least 17 species in southern Africa, including Viscum verrucosum [15]. Viscum verrucosum Harv. (Viscaceae) forms a leafless aerial shrub 0.5–1 m tall in host trees [16]. Flowering occurs in the dry season, mainly September–October, but fruits found throughout most of the year. Viscum verrucosum is found in mixed woodlands and bushlands at altitude ranging between 500 and 1 550 m. Host range in V. verrucosum is narrow, preferring high nutrient hosts mainly Vachellia species, but also on Ficus, Combretum and Syzygium species [17]. In addition to providing nutritive and highly digestible dry-season browse for livestock in savanna rangelands [18], [19], V. verrucosum also contributes significantly to carbon and nutrient cycling in semi-arid savanna [20], [21], [22].

In this study, we analyzed the patterns of random amplified polymorphic DNA (RAPD) variation of Viscum verrucosum populations in semi-arid savanna, south-western Zimbabwe. Our main study objectives were to: (i) determine genetic variability among and within V. verrucosum populations and (ii) examine the relative role of geographical distance in determining the patterns of genetic variation among populations.