Christopher J. Neufeld

Summary: 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.

Marine heatwaves (MHWs), increasing in duration and intensity because of climate change, are now a major threat to marine life and can have lasting effects on the structure and function of ecosystems. However, the responses of marine taxa and ecosystems to MHWs can be highly variable, making predicting and interpreting biological outcomes a challenge. Here, we review how biological responses to MHWs, from individuals to ecosystems, are mediated by fine‐scale spatial variability in the coastal marine environment (hereafter, local gradients). Viewing observed responses through a lens of ecological theory, we present a simple framework of three ‘resilience processes’ (RPs) by which local gradients can influence the responses of marine taxa to MHWs. Local gradients (1) influence the amount of stress directly experienced by individuals, (2) facilitate local adaptation and acclimatization of individuals and populations, and (3) shape community composition which then influences responses to MHWs. We then synthesize known examples of fine‐scale gradients that have affected responses of benthic foundation species to MHWs, including kelp forests, coral reefs, and seagrass meadows and link these varying responses to the RPs. We present a series of case studies from various marine ecosystems to illustrate the differential impacts of MHWs mediated by gradients in both temperature and other co‐occurring drivers. In many cases, these gradients had large effect sizes with several examples of local gradients causing a 10‐fold difference in impacts or more (e.g., survival, coverage). This review highlights the need for high‐resolution environmental data to accurately predict and manage the consequences of MHWs in the context of ongoing climate change. While current tools may capture some of these gradients already, we advocate for enhanced monitoring and finer scale integration of local environmental heterogeneity into climate models. This will be essential for developing effective conservation strategies and mitigating future marine biodiversity loss.

As on land, oceans exhibit high temporal and spatial temperature variation. This “ocean weather” contributes to the physiological and ecological processes that ultimately determine the patterns of species distribution and abundance, yet is often unrecognized, especially in tropical oceans. Here, we tested the paradigm of temperature stability in shallow waters (<12.5 m) across different zones of latitude. We collated hundreds of in situ, high temporal-frequency ocean temperature time series globally to produce an intuitive measure of temperature variability, ranging in scale from quarter-diurnal to annual time spans. To estimate organismal sensitivity of ectotherms (i.e. microbes, algae, and animals whose body temperatures depend upon ocean temperature), we computed the corresponding range of biological rates (such as metabolic rate or photosynthesis) for each time span, assuming an exponential relationship. We found that subtropical regions had the broadest temperature ranges at time spans equal to or shorter than a month, while temperate and tropical systems both exhibited narrow (i.e. stable) short-term temperature range estimates. However, temperature-dependent biological rates in tropical regions displayed greater ranges than in temperate systems. Hence, our results suggest that tropical ectotherms may be relatively more sensitive to short-term thermal variability. We also highlight previously unexplained macroecological patterns that may be underpinned by short-term temperature variability.

Kelp forests are among the most abundant coastal marine habitats but are vulnerable to the impacts of climate change. Between 2014 and 2016, an unprecedented heatwave and associated changes in trophic dynamics threatened kelp forests across the Northeast Pacific, with impacts documented from Mexico to Alaska. However, responses have varied substantially and remain poorly characterized across large stretches of coast, especially British Columbia (B.C.), which represents a significant percentage of the range of floating kelp species in the Northeast Pacific. Here, we explore variation in floating kelp ( Macrocystis, Nereocystis ) persistence pre- and post-heatwave across a >675 km latitudinal gradient, asking whether B.C. kelp forests are of conservation concern. We assembled and analyzed available quantitative kelp data, comparing snapshots of kelp extent before (1994 – 2007) and after (2018 – 2021) the heatwave in 11 regions spanning a range of temperature and sea otter-occupancy statuses, and contextualizing these with time series analyses, where available (n = 7 regions). We provide strong evidence that kelp forests have declined in many regions but with evidence of refugia at both local and regional scales. Kelp forest persistence was negatively correlated with summer sea temperatures in southern B.C., where temperatures varied by ~6°C across sites, at times exceeding species’ thermal tolerances. Kelp dynamics in northern regions appeared instead to be modulated by top-down control by urchins and sea otters. Our results demonstrate that B.C.’s kelp forest have been substantially reduced in recent years but that regional and local-scale factors influence the resilience of forests to large-scale perturbations.

Marine heatwaves threaten the persistence of kelp forests globally. However, the observed responses of kelp forests to these events have been highly variable on local scales. Here, we synthesize distribution data from an environmentally diverse region to examine spatial patterns of canopy kelp persistence through an unprecedented marine heatwave. We show that, although often overlooked, temperature variation occurring at fine spatial scales (i.e., a few kilometers or less) can be a critical driver of kelp forest persistence during these events. Specifically, though kelp forests nearly all persisted toward the cool outer coast, inshore areas were >3°C warmer at the surface and experienced extensive kelp loss. Although temperatures remained cool at depths below the thermocline, kelp persistence in these thermal refugia was strongly constrained by biotic interactions, specifically urchin populations that increased during the heatwave and drove transitions to urchin barrens in deeper rocky habitat. Urchins were, however, largely absent from mixed sand and cobble benthos, leading to an unexpected association between bottom substrate and kelp forest persistence at inshore sites with warm surface waters. Our findings demonstrate both that warm microclimates increase the risk of habitat loss during marine heatwaves and that biotic interactions modified by these events will modulate the capacity of cool microclimates to serve as thermal refugia.

Much of the morphological and ecological diversity present on earth is believed to have arisen through the process of adaptive radiation. Yet, this is seemingly at odds with substantial evidence that niches tend to be similar among closely related species (i.e. niche conservatism). Identifying the relative importance of these opposing processes in driving niche evolution under different circumstances is therefore essential to our understanding of the interaction between ecological and evolutionary phenomena. In this study, we make use of recent advances in our understanding of the phylogeny of kelps (Laminariales) to investigate niche evolution in one of the most ecologically significant groups of benthic habitat‐forming organisms on the planet. We quantify functional traits and use community sampling data from a kelp diversity hotspot to determine which traits are responsible for the habitat (β) niche of kelps and whether they are labile or conserved across the kelp phylogeny. We find that combinations of functional traits have evolved convergently across kelp subclades and that these functional traits are significant predictors of community structure. Specifically, traits associated with whole‐kelp structural reinforcement and material properties were found to be significantly correlated with species distributions along a gradient of wave disturbance and thus predict the outcome of environmental filtering. However, kelp assemblages were made up of species that are more phylogenetically distinct than expected (i.e. phylogenetic overdispersion), suggesting that niche partitioning along this gradient of wave disturbance has been an important driver of divergence between close relatives. These results are consistent with the hypothesis that environmental filtering associated with wave disturbance plays an essential role in determining the habitat niche of kelps across local communities and further suggest that this process can drive phenotypic divergence and niche partitioning between close relatives. We propose that parallel adaptive radiation of kelp subclades has shaped the diversity and species composition of kelp forests in the Northeast Pacific and we discuss how evidence from the literature on incipient or ongoing speciation events supports this hypothesis. A freePlain Language Summarycan be found within the Supporting Information of this article.

Much of the morphological and ecological diversity present on earth is believed to have arisen through the process of adaptive radiation. Yet, this is seemingly at odds with substantial evidence that niches tend to be similar among closely related species (i.e., niche conservatism). Identifying the relative importance of these opposing processes in different circumstances is therefore essential to our understanding of the interaction between ecological and evolutionary phenomena. In this study, we make use of recent advances in our understanding of the phylogeny of kelps (Laminariales) to investigate niche evolution in one of the most important groups of benthic habitat-forming organisms on the planet. We quantify functional traits and use community sampling data from a kelp diversity hotspot to determine which traits are responsible for the habitat (β) niche of kelps and whether they are labile or conserved across the kelp phylogeny. We find that combinations of functional traits have evolved convergently across kelp subclades and that these traits are significant predictors of community structure. Specifically, traits associated with whole-kelp structural reinforcement and material properties were found to be significantly correlated with species distributions along a gradient of wave disturbance and thus predict the outcome of environmental filtering. However, kelp assemblages were made up of species that are more phylogenetically distinct than predicted from null models (i.e., phylogenetic overdispersion), suggesting that niche partitioning along this gradient of wave disturbance has been an important driver of divergence between close relatives. These results collectively demonstrate that environmental filtering by waves plays an essential role in determining the habitat niche of kelps across local communities and further suggest that this community-level process can drive phenotypic divergence between close relatives. We propose that parallel adaptive radiation of kelp subclades has shaped the diversity and species composition of kelp forests in the Northeast Pacific and we discuss how evidence from the literature on incipient or ongoing speciation events support this hypothesis.

Biodiversity loss is driven by interacting factors operating at different spatial scales. Yet, there remains uncertainty as to how fine-scale environmental conditions mediate biological responses to broad-scale stressors. We surveyed intertidal rocky shore kelp beds situated across a local gradient of wave action and evaluated changes in kelp diversity and abundance after more than two decades of broad scale stressors, most notably the 2013–2016 heat wave. Across all sites, species were less abundant on average in 2017 and 2018 than during 1993–1995 but changes in kelp diversity were dependent on wave exposure, with wave exposed habitats remaining stable and wave sheltered habitats experiencing near complete losses of kelp diversity. In this way, wave exposed sites have acted as refugia, maintaining regional kelp diversity despite widespread local declines. Fucoids, seagrasses and two stress-tolerant kelp species (Saccharina sessilis, Egregia menziesii) did not decline as observed in other kelps, and the invasive species Sargassum muticum increased significantly at wave sheltered sites. Long-term monitoring data from a centrally-located moderate site suggest that kelp communities were negatively impacted by the recent heatwave which may have driven observed losses throughout the region. Wave-sheltered shores, which saw the largest declines, are a very common habitat type in the Northeast Pacific and may be especially sensitive to losses in kelp diversity and abundance, with potential consequences for coastal productivity. Our findings highlight the importance of fine-scale environmental heterogeneity in mediating biological responses and demonstrate how incorporating differences between habitat patches can be essential to capturing scale-dependent biodiversity loss across the landscape.

Biodiversity loss is driven by interacting factors operating at different spatial scales. Yet, there remains uncertainty as to how fine-scale environmental conditions mediate biological responses to broad-scale stressors. We surveyed mid-latitude kelp bed habitats to determine whether local habitat heterogeneity has mediated changes in community diversity after more than two decades of extreme temperature events, most notably the 2013-2016 heat wave. Local wave exposure conditions were key in determining responses, with some habitats remaining stable and others experiencing near complete diversity loss, leading to local declines without regional extinctions. Wave-sheltered shores, which saw the largest declines, are a very common habitat type in the Northeast Pacific and may be especially sensitive to climate-related losses in kelp diversity and abundance. Our findings highlight how local gradients can interact with global drivers to facilitate diversity loss and demonstrate how incorporating differences between habitat patches can be essential to capturing scale-dependent biodiversity loss across the landscape.

Species–area relationships (SARs) are among the most general patterns in nature. Yet, significant variation in species richness often remains after accounting for area, especially for small islands. One factor thought to influence species richness on small islands is disturbance from the combined influence of tides and waves. Here, we derive a quantitative framework for determining how ocean disturbance impacts island communities, which we then test in plant communities in a temperate island archipelago. We do so by applying some well‐developed techniques honed in the marine intertidal zone but rarely applied to studies on land. By estimating and adjusting for the effect of wave exposure on habitable island area, we dramatically improved the fit of the SAR for small islands, nearly doubling the amount of variation in species richness explained (from 37% to 69%). Our predictions of island occupancy also improved using this method. Our approach predicts that small islands (2) are the most affected by ocean‐borne disturbance. Given that many archipelagos are susceptible to wave disturbance, future studies should consider how ocean‐borne disturbances arising from the matrix might interact with sampling area to influence patterns of species richness on small islands.