Metapopulation extinction caused by mutation accumulation

Abstract

Theory suggests that the risk of extinction by mutation accumulation can be comparable to that by environmental stochasticity for an isolated population smaller than a few thousand individuals. Here we show that metapopulation structure, habitat loss or fragmentation, and environmental stochasticity can be expected to greatly accelerate the accumulation of mildly deleterious mutations, lowering the genetic effective size to such a degree that even large metapopulations may be at risk of extinction. Because of mutation accumulation, viable metapopulations may need to be far larger and better connected than would be required under just stochastic demography. K imura, Maruyama, and Crow (1) first noted that mildly deleterious mutations may create a considerably larger mutational load in small populations than more deleterious mutations. Deleterious mutations impose a load on populations through a reduction in the mean survivorship and͞or reproductive rates of individuals (2-5). In very large, effectively infinite populations, an equilibrium mutation load exists that is independent of the mutational effect (2, 3, 5, 6). However, in sufficiently small isolated populations, mildly deleterious mutations may be a potent extinction force, because individually they are nearly invisible to natural selection, although causing an appreciable cumulative reduction in population viability (1,5,(7)(8)(9)(10)(11). Theory suggests that the accumulation of mildly deleterious mutations can be comparable to environmental stochasticity in causing extinction of populations smaller than a few thousand individuals (8,12,13).All previous theoretical work on extinction caused by mutation accumulation has focused on a single panmictic population, but most populations have some degree of subdivision, which may greatly magnify the stochastic development of mutation load (14,15). Moreover, most theoretical work on extinction has focused on only one or two extinction mechanisms at a time, for reasons of mathematical tractability. But demographic (16, 17), environmental (16, 17), and genetic stochasticity (8, 10, 11) operate simultaneously in natural populations, and their synergy may have a strong impact on the probability of extinction (12,13,(18)(19)(20)(21)(22). Genetic and Demographic ModelWe simulate the dynamics of metapopulation extinction using a biologically realistic model that includes stochastic demographic (17, 23), environmental (17, 23), and genetic (24) mechanisms. Our individual-based model (25) includes population dynamics within each patch, explicit spatial structure, and an explicit representation of each diploid genome (10,11,17,23,24).We parameterize the genetic mechanisms in our model using values from a broad array of empirical studies. Independent data on a diversity of organisms suggest that the genomic deleterious mutation rate, U, is frequently on the order of 0.1 to 1 per individual per generation in multicellular eukaryotes, and that the average homozygous and heterozygous effects of such mutations are typically le...

Population signatures of large-scale, long-term disjunction and small-scale, short-term habitat fragmentation in an Afromontane forest bird

“…Ultimately, the combination of habitat loss, deterioration and isolation is expected to modify the ecological conditions for populations, which have been shown to be subject to stochastic demographic fluctuations, increased inbreeding, loss of heterozygosity and accumulation of mildly deleterious alleles. Genetic variation might additionally be lost through strong genetic drift in exceedingly small populations (Frankham, 1995;Higgins and Lynch, 2001;Keller and Waller, 2002;Kalinowski and Waples, 2002;Frankham, 2005;Palstra and Ruzzante, 2008). The direction and strength of these effects, however, are expected to vary with both the (evolutionary) history of the landscape and with species-specific life history traits (Callens et al, 2011;MacDougall-Shackleton et al, 2011).…”

Genetic consequences of population subdivision: the marsupial Micoureus paraguayanus (Mammalia: Didelphimorphia) as a case study

“…Loss of gene diversity over 100 years from metapopulations of M. paraguayanus with carrying capacity of 100 (3) and 2000 (4), divided into 1 ( ), 2 ( ), 5 ( ) or 10 ( ) subpopulations connected by different migration rates (0%, 1% or 5%) and by equal dispersal by both sexes (white) and male-biased dispersal (black). LYNCH 2001), lowering the genetic effective size to such a degree that even large metapopulations may be at risk of extinction (LANDE 1995, HIGGINS & LYNCH 2001. Because of mutation accumulation, viable metapopulations may need to be far larger and better connected than would be required under just demographic stochasticity (HIGGINS & LYNCH 2001).…”

“…LYNCH 2001), lowering the genetic effective size to such a degree that even large metapopulations may be at risk of extinction (LANDE 1995, HIGGINS & LYNCH 2001. Because of mutation accumulation, viable metapopulations may need to be far larger and better connected than would be required under just demographic stochasticity (HIGGINS & LYNCH 2001). From a genetic perspective, a metapopulation may be much more vulnerable to extinction than a population of the same overall number of individuals (HIGGINS & LYNCH 2001).…”

“…Because of mutation accumulation, viable metapopulations may need to be far larger and better connected than would be required under just demographic stochasticity (HIGGINS & LYNCH 2001). From a genetic perspective, a metapopulation may be much more vulnerable to extinction than a population of the same overall number of individuals (HIGGINS & LYNCH 2001). BRITO & FERNANDEZ (2000b) estimated that genetic stochasticity and inbreeding depression might be one of the most serious threats to the long-term persistence of a M. paraguayanus metapopulation composed of very small populations in southeastern Brazil.…”

Genetic and demographic dynamics of small populations of Silene latifolia

“…Therefore, the viability of many naturally fragmented populations may also be influenced by the interaction of genetics and demography (Richards, 2000a). This could be true at the level of the local population or at the level of the metapopulation, depending on the number and connectivity of local populations Higgins and Lynch, 2001).…”