Founder effects and species introductions: A host versus parasite perspective

Abstract

Species colonizations (both natural and anthropogenic) can be associated with genetic founder effects, where founding populations demonstrate significant genetic bottlenecks compared to native populations. Yet, many successfully established free-living species exhibit little reduction in genetic diversity-possibly due to multiple founding events and/or high propagule pressure during introductions. Less clear, however, is whether parasites may show differential signatures to their free-living hosts. Parasites with indirect life cycles may particularly be more prone to founder effects (i.e., more genetically depauperate) because of inherently smaller founding populations and complex life cycles. We investigated this question in native (east coast) and introduced (west coast) North American populations of a host snail Tritia obsoleta (formerly Ilyanassa obsoleta, the eastern mudsnail) and four trematode parasite species that obligately infect it. We examined genetic diversity, gene flow, and population structure using two molecular markers (mitochondrial and nuclear) for the host and the parasites. In the host snail, we found little to no evidence of genetic founder effects, while the trematode parasites showed significantly lower genetic diversity in the introduced versus native ranges. Moreover, the parasite's final host influenced infection prevalence and genetic diversity: Trematode species that utilized fish as final hosts demonstrated lower parasite diversity and heightened founder effects in the introduced range than those trematodes using birds as final hosts. In addition, inter-regional gene flow was strongest for comparisons that included the putative historical source region (mid-Atlantic populations of the US east coast). Overall, our results broaden understanding of the role that colonization events (including recent anthropogenic introductions) have on genetic diversity in non-native organisms by also evaluating less studied groups like parasites.

Keywords: gene flow; genetic bottleneck; introduction vector; invasion; life cycle; propagule pressure; trematode.

Figure 1

Theoretical schematic for the differences in (a) hosts and (b) parasites with indirect life cycles that may lead to differential genetic diversity in their founding regions. For (a) hosts, source genetic diversity and propagule pressure will affect the extent of the genetic bottleneck in a founding region, and therefore the genetic diversity in the region. For (b) parasites with indirect life cycles, life cycle complexity (e.g., multi‐host trophically transmitted parasites) and availability of suitable hosts will additionally affect bottlenecks and founding diversity. Each triangle depicts the directional change in genetic diversity (width) with increase (from top to bottom) in the individual factors labeled at top. Parasite life cycles include additional factors that modify diversity in founding populations. This figure has been adapted from figure 1 in Roman and Darling (2007) and figure 7.2 in Blakeslee (2016) with permission from the authors

Figure 2

Sample locations in the introduced Pacific and native Atlantic regions of Tritia obsoleta and four of its trematode parasites. In the native region, small black circles represent the North subregion; black diamonds represent the Source subregion; and black squares represent the South subregion. In the introduced region, red crosses represent Boundary Bay (BB), red diamonds represent Willapa Bay (WB), and red stars represent San Francisco Bay (SFB). Numbers represent those sites included in genetic analyses (sites are identified in Appendix S1B); all other sites on the map were sampled for parasite prevalence and richness only (see Blakeslee et al., 2012). Haplotype (COI) frequencies for T. obsoleta and trematode parasites are portrayed as pie charts, with pie piece coloring defined in the Key. Trematode pie charts are distinguished by an orange border. In some sites, we were unable to pair T. obsoleta and trematode haplotype data due to small sample size for the trematodes (i.e., sites where prevalence of infection was low). In the key, “North only,” “Source only,” and “South only” refer to haplotypes found at a site that were only found in a particular subregion; “North & Source” and “Source & South” refer to haplotypes in sites that were found in both the North and Source subregions, or the Source & South subregions (note: there were no haplotypes found at any site that were shared between just the North & South subregions); “Ubiquitous” represents haplotypes found across all three subregions; and “Unique to site” refers to haplotypes only found in a particular site. Figure modified from Blakeslee et al. (2012) with the authors’ permissions

Figure 3

Pie chart representations of proportional haplotype richness and frequency based on the COI marker for the host, Tritia obsoleta, and four of its trematode parasites (Austrobilharzia variglandis, Himasthla quissitensis, Lepocreadium setiferoides, Zoogonus lasius). Three separate comparisons are made for proportional haplotype richness and frequency: left—T. obsoleta, the host snail; middle—all four trematode parasites collectively; right—trematodes divided into bird‐using (AV and HQ) and fish‐using (LS and ZL) groups. For both the left and middle panels, the left pie charts compare the introduced versus entire native region, and the right compares the introduced region to just the source area of native region; the far right panel compares the whole native region to the introduced region for different definitive hosts. Black pie pieces = haplotypes only found in the native (N) or Source (S) regions; white pie pieces = haplotypes only found in the introduced (I) region; gray patterned pieces = haplotypes shared between the regions. For haplotype frequencies: black‐patterned pieces = occurrences of shared haplotypes across native and introduced that are found in the native or Source regions (shared‐native); white‐patterned pieces = occurrences of shared haplotypes that are found in the introduced region (shared‐introduced)

Figure 4

Haplotype network depicting COI maker of the four trematode parasites (Austrobilharzia variglandis [AV], Himasthla quissitensis [HQ], Lepocreadium setiferoides [LS], Zoogonus lasius [ZL]) of Tritia obsoleta in the native and introduced regions, and 18S marker of HQ. Colors represent different subregions in the native and introduced regions. Shading depicts the different trematode species and genetically distinct lineages (HQ‐1, HQ‐2, HQ‐3, LS‐1, and LS‐2) based on a Bayesian phylogenetic tree (Figure S3). The inset represents the analysis for HQ using the 18S marker. See Table 1 for subregion abbreviations and trematode species abbreviations

Figure 5

Migration rates among native subregions and the introduced region for Tritia obsoleta. This demonstrates the rate of gene flow based on marginal peak probabilities using the isolation with migration model (IMa) (Hey & Nielsen, 2007). Migration rates are presented as region 1 → region 2 (black) or region 2 → region 1 (gray). For example, in the first comparison, the black bar represents gene flow from the Source subregion to the introduced region, while the gray bar represents gene flow from the introduced region to the Source subregion. Significant post hoc comparisons are represented as letters above the bars. The results suggest strong directional flow from the Source subregion to the introduced region, with little evidence of gene flow to the introduced region from the North and South subregions. Other intra‐ and inter‐regional comparisons for T. obsoleta and also the parasite HQ can be found in Figure S6