Population genomics reveals strong impacts of genetic drift without purging and guides conservation of bull and giant kelp

Kelp forests are declining in many parts of the northeast Pacific.1,2,3,4 In small populations, genetic drift can reduce adaptive variation and increase fixation of recessive deleterious alleles,5,6,7 but natural selection may purge harmful variants.8,9,10 To understand evolutionary dynamics and inform restoration strategies, we investigated genetic structure and the outcomes of genetic drift and purging by sequencing the genomes of 429 bull kelp (Nereocystis luetkeana) and 211 giant kelp (Macrocystis sp.) from the coastlines of British Columbia and Washington. We identified 6 to 7 geographically and genetically distinct clusters in each species. Low effective population size was associated with low genetic diversity and high inbreeding coefficients (including increased selfing rates), with extreme variation in these genetic health indices among bull kelp populations but more moderate variation in giant kelp. We found no evidence that natural selection is purging putative recessive deleterious alleles in either species. Instead, genetic drift has fixed many such alleles in small populations of bull kelp, leading us to predict (1) reduced within-population inbreeding depression in small populations, which may be associated with an observed shift toward increased selfing rate, and (2) hybrid vigor in crosses between small populations. Our genomic findings imply several strategies for optimal sourcing and crossing of populations for restoration and aquaculture, but these require experimental validation. Overall, our work reveals strong genetic structure and suggests that conservation strategies should consider the multiple health risks faced by small populations whose evolutionary dynamics are dominated by genetic drift. [Display omitted] •Small populations of bull and giant kelp face multiple genetic health risks•Genetic drift, but not purging, strongly impacts evolution in small populations•Strong genetic drift has reduced inbreeding depression within small populations•Genomics insights inform conservation and restoration of declining kelp species Bemmels et al. sequence >600 whole genomes of two canopy-forming kelp species undergoing decline. Small populations experience multiple genetic health risks but no purging of harmful alleles. Instead, genetic drift is likely reducing inbreeding depression. Evolutionary dynamics and genetic structure suggest conservation strategies for these taxa.