Genetic analyses of historic and modern marbled murrelets suggest decoupling of migration and gene flow after habitat fragmentation

Abstract

The dispersal of individuals among fragmented populations is generally thought to prevent genetic and demographic isolation, and ultimately reduce extinction risk. In this study, we show that a century of reduction in coastal old-growth forests, as well as a number of other environmental factors, has probably resulted in the genetic divergence of marbled murrelets (Brachyramphus marmoratus) in central California, despite the fact that 7 per cent of modern-sampled murrelets in this population were classified as migrants using genetic assignment tests. Genetic differentiation appears to persist because individuals dispersing from northern populations contributed relatively few young to the central California population, as indicated by the fact that migrants were much less likely to be members of parent-offspring pairs than residents (10.5% versus 45.4%). Moreover, a recent 1.4 per cent annual increase in the proportion of migrants in central California, without appreciable reproduction, may have masked an underlying decline in the resident population without resulting in demographic rescue. Our results emphasize the need to understand the behaviour of migrants and the extent to which they contribute offspring in order to determine whether dispersal results in gene flow and prevents declines in resident populations.

Figure 1.

Historic (pre-European settlement; hatched areas) and current (green areas) distribution of potential murrelet nesting habitat in northwestern North America. The map of the distribution of murrelet habitat from Oregon to Alaska was developed by Inforain's rainforest mapping project (http://www.inforain.org/rainforestatlas/rainforestatlas/page4.html), and the distribution of murrelet habitat in California was developed by Fox (1996). Also depicted are sample sizes for genetic analyses (n_mod = modern sample size, n_his = historic sample size), estimates of effective population size (N_e), and estimates of genetic population differentiation (F_ST) for marbled murrelets (B. marmoratus) sampled at five locations (solid red circles and red line) during both modern (1997–2007) and historic (1888–1940) sampling periods. Sampling locations included southeast Alaska (AK), British Columbia/Washington (BC/WA), Oregon (OR), northern California (NC) and central California (CC).

Figure 2.

Observed and expected population structure (F_ST) at nine microsatellite loci between marbled murrelets (B. marmoratus) sampled in central California versus northern California–southeast Alaska, based on a range of possible effective population sizes (N_e) and number of migrants per generation (N_em) for central California (open circle, expected F_ST when N_em = 0 for a given N_e; filled grey circle, expected F_ST when N_em = 5 for a given N_e; filled black circle, observed F_ST and N_e in central California).

Figure 3.

Estimates of population size (open circle, ±1 s.e.) and the proportion (filled black circle, ±1 s.e.) of migrant marbled murrelets (B. marmoratus) in central California in 1999–2003 and 1997–2003, respectively.

Figure 4.

Statistical power to detect 1–10% annual declines in the resident central California marbled murrelet (B. marmoratus) population, with and without a 1.4% annual increase in the proportion of migrants in the population, using estimates of abundance from at-sea surveys collected from 1999 to 2003 (filled black circle, 1.4% annual increase in migration; open circle, no migration).