Inbreeding depression in urban environments of the bird's nest fungus Cyathus stercoreus (Nidulariaceae: Basidiomycota)

Abstract

Many organisms display codispersal of offspring, but fewer display codispersal of compatible gametes. This mechanism enhances the ability of a species to colonize after long distance dispersal as a mechanism of reproductive assurance, but it also fosters inbreeding and potential reduction in fitness. Here we investigated both long distance dispersal and inbreeding in the bird's nest fungus Cyathus stercoreus, a dung and mulch-associated fungus with a splash cup fruiting body appearing like a miniature bird's nest of 'eggs' or peridioles that contain thousands of mating compatible meiotic spores. To investigate the genetic structure in the species, six North American urban populations were hierarchically sampled and genotyped using 10 microsatellite markers. We detected significant levels of inbreeding through heterozygote deficiencies at four loci, with global FIS=0.061. Dispersal limitation was suggested by both spatial autocorrelation and the detection of population structure between Louisiana and Michigan using clustering and F-statistics. Although inbreeding may facilitate colonization by the fungus, it has a negative effect on the fitness of populations as estimated from a 15% reduction in growth rates of inbred strains relative to outcrossed. Mating tests revealed that C. stercoreus has a higher estimated number of mating-type alleles (MAT-A= 39, MAT-B= 24) than other species of bird's nest fungi, which would increase its outcrossing efficiency. We speculate that the increased number of mating-type alleles is the result of a recent range and population size expansion into urban environments.

Figure 1

Graphical display of the posterior probabilities of the STRUCTURE analysis. Shown is the run with the highest posterior probability and K=2. Each bar represents the posterior probability of assignment of a single individual to one of two populations. Data were generated using the correlated-allele frequency model with admixture and sampling locations used as priors. Populations are labeled according to Table 1.

Figure 2

Auto-correlograms of distance by relatedness for Louisiana (a) and Michigan (b) populations. Points represent maximum distance of pairs of samples for that class. Line indicates the best fit line. Error bars indicate s.e.m. Fij values among the 10 loci. The correlation of distance and relatedness was tested by permutation of locations among genotypes, which was significant only for the Louisiana population (P<0.05).

Figure 3

Boxplot of growth rates of inbred and outbred C. stercoreus dikaryons. Thick lines indicate the median of each group, and the boxes surround the second and third quartiles of the data. The whiskers represent the minimum and maximum values excluding outliers, which are indicated as distinct points.

Figure 4

Results from the interstrain cross of 40 different haploid cultures derived from 12 fruiting bodies collected from Ann Arbor, MI (2,3,12), East Lansing, MI (4,5,6,7,9), Grand Valley, MI (1,8,11) and Edmonton CAN (10).+, compatible mating, A, incompatibility because of common MAT-A allele, B, incompatibility because of common MAT-B allele.