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

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Abstract

Kelp forests are declining in many parts of the northeast Pacific 1–4 . In small populations, genetic drift can reduce adaptive variation and increase fixation of recessive deleterious alleles 5–7 , but natural selection may purge harmful variants 8–10 . 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 pyrifera sensu lato 11 ; cf. 12 ) from the coastlines of British Columbia and Washington. We identified 6-7 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 vigour in crosses between small populations. Our genomic findings imply several strategies for optimal sourcing and crossing of populations for restoration and aquaculture, but which 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.

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  1. We expected that purging wouldremove putatively deleterious alleles from small populations but have no effect on frequenciesof alleles in less deleterious categorie

    I'm a little confused by this statement. This would make sense in certain cases (e.g., highly recessive mutations). But SNPeff and GERP scores give no information on recessiveness. If these are just any deleterious variants, then the expectation should be the opposite, that high Ne pops should purge load easier.

  2. Bull kelp and giant kelp are the principal canopy-forming species in kelp forests of thenortheast Pacific, supporting highly productive and biodiverse ecosystems13

    I really liked reading this paper. It's great to see such detailed sampling and interrogation of the pop-gen of these keystone species.

  3. A strong isolation-by-distance pattern of increasing genetic distance (dXY) with geographic distance (Figure S4) andthe presence of populations admixed between clusters (Figure 1A-D) suggest that adjacentclusters are connected by gene flow.

    Seems in bull kelp lots of gene flow occurs across the southern tip of Vancouver Island. On the other hand, the northern tip seems to represent a barrier (judging by the clusters in Fig1). Are there any hydrological/oceanographic reasons to expect this maybe?

  4. We estimatedeffective population size (Ne)

    Does this mean you report selfing Ne (rather than typical coalescent Ne) in your analyses? This would be useful to highlight in the main text.

    1. All else being equal, indivi

    Is there any correlation in Ne/inbreeding/low diversity between the two species of help where they co-occur? This could be a useful indicator for conservation efforts.

  5. such as in recently bottlenecked populations

    Does this seem plausible in the case of kelp? If bottlenecking has been recent, the effect on Ne will be instant, but it will take for the signal of differences in purging to build up. Have strong kelp declines been more recent (>50 years)?

  6. We observed no evidence of purging in either species. We predicted that smallerpopulations would show a reduction in DMA frequency at evolutionarily conserved sites (GERPanalysis) due to increased homozygosity and exposure to selection, yet DMA frequency wasuncorrelated with population size (Figure 3A-B)

    While there are no differences between populations, the regression lines for the GERP/SNPeff analyses clearly show that less constrained sites harbor more diversity than more constrained sites, implying that purifying selection is acting on purging deleterious variants in both species. Seems like purging is present in this dataset it is more of a time-scale issue when it comes to detecting it. This makes sense particularly for recessive variants since they will be hidden from selection for a lot of time.