Gene flow from an adaptively divergent source causes rescue through genetic and demographic factors in two wild populations of Trinidadian guppies

Abstract

Genetic rescue, an increase in population growth owing to the infusion of new alleles, can aid the persistence of small populations. Its use as a management tool is limited by a lack of empirical data geared toward predicting effects of gene flow on local adaptation and demography. Experimental translocations provide an ideal opportunity to monitor the demographic consequences of gene flow. In this study we take advantage of two experimental introductions of Trinidadian guppies to test the effects of gene flow on downstream native populations. We individually marked guppies from the native populations to monitor population dynamics for 3 months before and 26 months after gene flow. We genotyped all individuals caught during the first 17 months at microsatellite loci to classify individuals by their genetic ancestry: native, immigrant, F1 hybrid, F2 hybrid, or backcross. Our study documents a combination of demographic and genetic rescue over multiple generations under fully natural conditions. Within both recipient populations, we found substantial and long-term increases in population size that could be attributed to high survival and recruitment caused by immigration and gene flow from the introduction sites. Our results suggest that low levels of gene flow, even from a divergent ecotype, can provide a substantial demographic boost to small populations, which may allow them to withstand environmental stochasticity.

Keywords: Poecilia reticulata; capture‐mark‐recapture; demographic rescue; fitness; gene flow; genetic rescue; hybridization; population growth.

Figure 1

(A) Schematic of the introduction scenario that allowed us to test the effects of gene flow from guppies that originated from an adaptively divergent source population (red) into two native populations (blue). (B) Principal components analyses using microsatellite data highlights initial genetic divergence between the native populations (blue) and the source of the introductions (red). (C) Principal component analyses using phenotypic traits highlights initial phenotypic divergence between native populations and the source of the introductions. Traits included in this analysis were male life history and body shape traits from data published in Fitzpatrick et al. (2015).

Figure 2

Temporal changes in within‐population genetic diversity following the introductions upstream that occurred in March 2009, as indicated by the red arrow. Solid lines correspond to heterozygosity (scale on left vertical axis) and dashed lines correspond to allelic richness (scale on right vertical axis). Genetic diversity indices were calculated using genotypes from all individuals caught in a given month.

Figure 3

Thick black lines indicate total number of guppies >14 mm captured in each stream over time. Gray boxes correspond to the timeframe in which every individual was genotyped at microsatellite loci for classification into genetic ancestry groups. Colors show the number of individuals in each genetic group caught each month.

Figure 4

Monthly population growth rate estimates and 95% confidence intervals for males and females from Caigual and Taylor streams throughout the entire duration of study. Estimates are based on capture‐mark‐recapture data and the best‐supported Pradel model (Tables S3).

Figure 5

Estimates and 95% confidence intervals of male and female survival probability of different genetic ancestry classifications in Caigual (A) and Taylor (B). All estimates are based on capture‐mark‐recapture data from the first 17 months of the study when all individuals were genotyped and classified into genetic groups. Estimates from the best‐supported Pradel model were plotted (see Tables S4 and S5).

Figure 6

Recruitment estimates and 95% confidence intervals of different genetic ancestry classifications in Caigual and Taylor. All estimates are based on capture‐mark‐recapture data from the first 17 months of the study when all individuals were genotyped and classified into genetic groups. Estimates from the best‐supported Pradel model were plotted (see Tables S4 and S5).