David O. Conover

Chromosomal inversions are often implicated in divergence between distinct ecotypes, but their role in maintaining continuous adaptive divergence in complex traits remains poorly understood. Using quantitative and population genetics, transcriptomics, and artificial selection experiments, we demonstrate how inversions enable clinal adaptive divergence along a steep environmental gradient despite extensive gene flow in a widely distributed marine fish. We show that three inversions are associated with multiple adaptive traits and harbor the strongest signatures of divergent selection in the genome, implying a crucial adaptive role. These inversions exhibit contrasting selection signatures across latitudes, suggesting that they control distinct aspects of the same complex traits and facilitate adaptation in a modular way to different environmental pressures despite gene flow.

My career is inextricably linked to the remarkable characteristics and astonishing insights provided by a simple yet elegant species, the Atlantic silverside, Menidia menidia. My initial field and laboratory studies provided the first demonstration of temperature-dependent sex determination (TSD) and its adaptive significance in fish, as well as the first empirical confirmation of frequency-dependent sex ratio selection. This early work then led to the discovery of countergradient variation in growth, evolutionary trade-offs associated with growth, pioneered the study of fisheries-induced evolution, and furthered our understanding of the spatial scale of local adaptation in marine species. Most of these topics are now vigorous areas of research encompassing numerous species and systems. Here I describe how these unforeseen discoveries were made and led to other findings on bluefish (Pomatomus saltatrix) and striped bass (Morone saxatilis). An interest in leadership during my early years was later rekindled as I took on administrative roles. It all began with an intriguing observation stemming from my MS thesis that I was compelled to follow. My career illustrates the value of exploring deeply the natural history of lesser-known yet easy-to-study species and to follow unexpected observations even if peripheral to a preconceived plan of research.

The study of local adaptation in the presence of ongoing gene flow is the study of natural selection in action, revealing the functional genetic diversity most relevant to contemporary pressures. In addition to individual genes, genome‐wide architecture can itself evolve to enable adaptation. Distributed across a steep thermal gradient along the east coast of North America, Atlantic silversides (Menidia menidia) exhibit an extraordinary degree of local adaptation in a suite of traits, and the capacity for rapid adaptation from standing genetic variation, but we know little about the patterns of genomic variation across the species range that enable this remarkable adaptability. Here, we use low‐coverage, whole‐transcriptome sequencing of Atlantic silversides sampled along an environmental cline to show marked signatures of divergent selection across a gradient of neutral differentiation. Atlantic silversides sampled across 1371 km of the southern section of its distribution have very low genome‐wide differentiation (median F_ST = 0.006 across 1.9 million variants), consistent with historical connectivity and observations of recent migrants. Yet almost 14,000 single nucleotide polymorphisms (SNPs) are nearly fixed (F_ST > 0.95) for alternate alleles. Highly differentiated SNPs cluster into four tight linkage disequilibrium (LD) blocks that span hundreds of genes and several megabases. Variants in these LD blocks are disproportionately nonsynonymous and concentrated in genes enriched for multiple functions related to known adaptations in silversides, including variation in lipid storage, metabolic rate, and spawning behavior. Elevated levels of absolute divergence and demographic modeling suggest selection maintaining divergence across these blocks under gene flow. These findings represent an extreme case of heterogeneity in levels of differentiation across the genome, and highlight how gene flow shapes genomic architecture in continuous populations. Locally adapted alleles may be common features of populations distributed along environmental gradients, and will likely be key to conserving variation to enable future responses to environmental change.

Parallel and idiosyncratic fish adaptation: Fish populations respond rapidly to fishing pressure. Within a handful of generations, marked phenotypic change can occur—often to smaller body sizes, because it is the big fish that are usually extracted. Therkildsen et al. examined wild ancestor fish lineages and found that polygenic mechanisms underpin this rapid evolutionary capacity (see the Perspective by Jørgensen and Enberg). Phenotypic change happened in two ways: first, by multiple small parallel changes in hundreds of unlinked genes associated with growth variation in the wild, and second, by shifts in large blocks of linked genes, causing large allele frequency changes at some loci. Science , this issue p. 487 ; see also p. 443