Stay at home aphids: comparative spatial and seasonal metapopulation structure and dynamics of two specialist tansy aphid species studied using microsatellite markers

Abstract

Two tansy-feeding aphids, Macrosiphoniella tanacetaria (MA) and Metopeurum fuscoviride (ME), were studied at a small spatial scale in and around Jena (< 80 km 2 ) using polymorphic microsatellite markers. Both species were found in approximately 60% of sites formerly known to harbour the aphids, although, generally when they did occur, they occurred singly (MA~50%; ME~60%) and rarely together on the same plant at the same time (approximately 10%) and then usually only in the early part of the growing season. This difference may be a result of quasi-apparent competition effects elicited by ants farming ME aphids, and preferentially actively eliminating or disturbing MA aphids. In terms of population genetics, both aphids showed extreme genetic heterogeneity within a metapopulation structure, with ME more than MA (i.e. higher FST values, approximately 0.4 versus 0.15, respectively), and limited levels of interpopulation gene flow. Subpopulations often deviated from Hardy-Weinberg equilibrium and showed linkage disequilibria, as expected in animals with extended parthenogenetic reproduction, and had positive FIS values for most large samples, suggesting inbreeding, and possibly philopatry, certainly in ME. Hierarchical analysis (allele range and number per locus, analysis of molecular variance and FST) strongly suggested that the plant rather than site governs the level of genetic variation. Bayesian clustering analysis revealed that both species had heterogeneous historical genetic patterning, with K (number of subgroups) in the range 3-7. Evidence is also provided from isolation-by-distance and private allele analyses indicating that, in MA, the presence of winged autumn males, absent in ME where males are wingless, influences comparative population genetic structuring, such that ME subpopulations are comparatively more inbred and genetically differentiated than MA subpopulations. Lastly, additional spatial arrangement (ALLELES-IN-SPACE) analysis showed that, in both species, certain subpopulations were genetically isolated from the remainder, probably as a result of geographical barriers, including intervening buildings and woods. As such, the biology of these tansy aphids living in semi-natural habitats is very different from many pest aphid species examined within agro-ecosystems and infesting ephemeral crops. This is because the former appear to be much more reluctant to fly and hence show contrastingly much higher levels of interpopulation divergence, even at small spatial scales as investigated in the present study. Indeed, the number of genotypic clusters found for tansy aphids using Bayesian approaches is similar to that globally for the major pest, the peach-potato aphid, Myzus persicae.

Differential Performance of <I>Sitobion avenae</I> Populations From Both Sides of the Qinling Mountains Under Common Garden Conditions

“…For example, the Green Mountain range in the United States was found to be a barrier to dispersal for the mosquito Anopheles punctipennis (Say), and affected the population structure of this species (Fairley et al 2000). Similar structuring effects of geographical barriers were found for the woolly apple aphid Eriosoma lanigerum (Hausmann) (Lavandero et al 2009), the tansy-feeding aphids (Macrosiphoniella tanacetaria (Kaltenbach) and Metopeurum fuscoviride Stroyan) (Loxdale et al 2011), and Russian wheat aphid (Diuraphis noxia Kurdjumov) (Zhang et al 2012). Interestingly, Russian wheat aphid showed clear geographic isolation between populations in northern and southern Xinjiang, probably because the Tianshan Mountain range segregates Xinjiang, China, into northern and southern regions (Zhang et al 2012).…”

Habitat variation, mutualism and predation shape the spatio‐temporal dynamics of tansy aphids

“…Another metapopulation model system comprises specialised aphids (Homoptera, Aphidoidea) on patchily distributed host plants (Addicott, 1978;Weisser, 2000;Loxdale et al, 2011). It is host to several specialised aphids such as Metopeurum fuscoviride Stroyan (Aphididae) that have been shown to exhibit metapopulation structuring, with aphid populations genetically structured more at the individual plant level than at the site level (Loxdale et al, 2011). These different clusters vary in size and can be easily distinguished in the field.…”

“…For example, the Asteraceae tansy (Tanacetum vulgare L.) is able to propagate by tussock-forming rhizome growth, leading to clusters of genetically identical shoots. Between sites, there is limited gene flow such that the different metapopulations are genetically differentiated (Loxdale et al, 2011). Local aphid populations (colonies) are confined to a particular plant individual and generally show low persistence times with extinction driven by top-down interactions with natural enemies (Weisser, 2000).…”

Multiple Cues for Winged Morph Production in an Aphid Metacommunity

“…In a metapopulation setting, dispersal is even more important as each plant is an ‘island of resource’ separated by unsuitable habitat that the aphids have to navigate before reaching the next suitable plant. Two specialist aphid species ( Macrosiphoniella tanacetaria and Metopeurum fuscoviride (Hemiptera: Aphididae)) on tansy ( Tanacetum vulgare (Asteraceae)) exhibit classic metapopulation structuring [37], [38], [39]. Metopeurum fuscoviride is tended by ants, which can protect aphids from predators and may inhibit wing production [5].…”