Host density drives the postglacial migration of the tree parasite, Epifagus virginiana

Abstract

To survive changes in climate, successful species shift their geographic ranges to remain in suitable habitats. For parasites and other highly specialized species, distributional changes not only are dictated by climate but can also be engineered by their hosts. The extent of host control on parasite range expansion is revealed through comparisons of host and parasite migration and demographic histories. However, understanding the codistributional history of entire forest communities is complicated by challenges in synthesizing datasets from multiple interacting species of differing datatypes. Here we integrate genetic and fossil pollen datasets from a host-parasite pair; specifically, the population structure of the parasitic plant (Epifagus virginiana) was compared with both its host (Fagus grandifolia) genetic patterns and abundance data from the paleopollen record of the last 21,000 y. Through tests of phylogeographic structure and spatial linear regression models we find, surprisingly, host range changes had little effect on the parasite's range expansion and instead host density is the main driver of parasite spread. Unlike other symbionts that have been used as proxies to track their host's movements, this parasite's migration routes are incongruent with the host and instead reflect the greater importance of host density in this community's assembly. Furthermore, these results confirm predictions of disease ecological models regarding the role of host density in the spread of pathogens. Due to host density constraints, highly specialized species may have low migration capacities and long lag times before colonization of new areas.comparative phylogeography | host-parasite interactions | eastern North America | Orobanchaceae | Fagus B ecause of species-specific interactions and obligate hostparasite relationships, many parasites are thought to closely track their hosts during range expansions. With their shorter generation times and more quickly evolving genomes, parasites can make attractive proxies for understanding host migration patterns (1, 2). However, parasite and host phylogeographic histories may be incongruent, and that conflict reflects processes that have limited the spread of the parasite relative to the host. In particular, host density has been implicated in disease systems as a constraint on parasite spread (3, 4). We take a historical approach to investigate the effects of host density on both population differentiation and postglacial migration in the assembly of a tree-herb, host-parasite system. The influence of changes in host range and host density on a parasite's migration history is examined by comparing the parasite phylogeography with both the host phylogeography (5) and host abundance data (6) over the last 21,000 y. Postglacial migration is approximately analogous to present-day range shifts due to climate change (7), so our approach can help to understand current factors controlling community assembly at different trophic levels.The eastern North American study system consists ...

A niche perspective on the range expansion of symbionts

“…Stanko, Krasnov & Morand, 2006;Almberg et al, 2012). Demographic and genetic data strongly suggest that the postglacial range expansion of the parasitic plant Epifagus virginiana was primarily driven by high population densities of its host Fagus grandifolia (Tsai & Manos, 2010). Evolution of symbiont life-history traits associated with dispersal is another potential driver of dispersal facilitation.…”

Conspecific negative density dependence in American beech

“…However, the direct effects of these aphids on beech seedlings are unknown, and it is possible that beech regeneration is more prone to aphid colonization when in close proximity to conspecific adults. Another possible cause of CNDD in American beech is Epifagus virginiana (beechdrops), a parasitic plant that persists exclusively on beech roots and is most common and abundant in areas of high beech density (Tsai and Manos 2010;Abbate and Campbell 2013). Like the preceding example, this parasite is not believed to cause significant damage to mature beech trees, but to the best of our knowledge no previous research has investigated its potential effects on beech regeneration.…”

A rangewide herbarium‐derived dataset indicates high levels of gene flow in black cherry (Prunus serotina)

“…Many other studies have indirectly addressed the notion of IBD in North American plants, often through the visual interpretation of the geographic array of DNA sequence haplotypes or multivariate genetic clusters. Thirteen of the 19 native plant taxa reviewed in Soltis, Morris, McLachlan, Manos, and Soltis () exhibited some level of geographic structure, as have numerous subsequent studies (Morris, Ickert‐Bond, Brunson, Soltis, & Soltis, ; Rodrigues & Stefanovic, ; Thomson, Dick, & Dayanandan, ; Tsai & Manos, ; Willyard et al, ; Zinck & Rajora, ). In contrast, many exotic species in North America do not exhibit IBD.…”