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Abstract Habitat transitions have shaped the evolutionary trajectory of many clades. Sea catfishes (Ariidae) have repeatedly undergone ecological transitions, including colonizing freshwaters from marine environments, leading to an adaptive radiation in Australia and New Guinea alongside non-radiating freshwater lineages elsewhere. Here, we generate and analyze one long-read reference genome and 66 short-read whole genome assemblies, in conjunction with genomic data for 54 additional species. We investigate how three major ecological transitions have shaped genomic variation among ariids over their ~ 50 million-year evolutionary history. Our results show that relatively younger freshwater lineages exhibit a higher incidence of positive selection than their more ancient marine counterparts. They also display a larger disparity in body shapes, a trend that correlates with a heightened occurrence of positive selection on genes associated with body size and elongation. Although positive selection in the Australia and New Guinea radiation does not stand out compared to non-radiating lineages overall, selection across the prolactin gene family during the marine-to-freshwater transition suggests that strong osmoregulatory adaptations may have facilitated their colonization and radiation. Our findings underscore the significant role of selection in shaping the genome and organismal traits in response to habitat shifts across macroevolutionary scales. 

Abstract Migration independently evolved numerous times in animals, with a myriad of ecological and evolutionary implications. In fishes, perhaps the most extreme form of migration is diadromy, the migration between marine and freshwater environments. Key and long-standing questions are: how many times has diadromy evolved in fishes, how frequently do diadromous clades give rise to non-diadromous species, and does diadromy influence lineage diversification rates? Many diadromous fishes have large geographic ranges with constituent populations that use isolated freshwater habitats. This may limit gene flow between some populations, increasing the likelihood of speciation in diadromous lineages relative to nondiadromous lineages. Alternatively, diadromy may reduce lineage diversification rates if migration is associated with enhanced dispersal capacity that facilitates gene flow within and between populations. Clupeiformes (herrings, sardines, shads, and anchovies) is a model clade for testing hypotheses about the evolution of diadromy because it includes an exceptionally high proportion of diadromous species and several independent evolutionary origins of diadromy. However, relationships among major clupeiform lineages remain unresolved, and existing phylogenies sparsely sampled diadromous species, limiting the resolution of phylogenetically informed statistical analyses. We assembled a phylogenomic dataset and used multi-species coalescent and concatenation-based approaches to generate the most comprehensive, highly resolved clupeiform phylogeny to date, clarifying associations among several major clades and identifying recalcitrant relationships needing further examination. We determined that variation in rates of sequence evolution (heterotachy) and base-composition (nonstationarity) had little impact on our results. Using this phylogeny, we characterized evolutionary patterns of diadromy and tested for differences in lineage diversification rates between diadromous, marine, and freshwater lineages. We identified 13 transitions to diadromy, all during the Cenozoic Era (10 origins of anadromy, 2 origins of catadromy, and 1 origin of amphidromy), and 7 losses of diadromy. Two diadromous lineages rapidly generated nondiadromous species, demonstrating that diadromy is not an evolutionary dead end. We discovered considerably faster transition rates out of diadromy than to diadromy. The largest lineage diversification rate increase in Clupeiformes was associated with a transition to diadromy, but we uncovered little statistical support for categorically faster lineage diversification rates in diadromous versus nondiadromous fishes. We propose that diadromy may increase the potential for accelerated lineage diversification, particularly in species that migrate long distances. However, this potential may only be realized in certain biogeographic contexts, such as when diadromy allows access to ecosystems in which there is limited competition from incumbent species. 

Abstract AimThe latitudinal diversity gradient of increasing species richness from poles to equator is one of the most striking and pervasive spatial patterns of biodiversity. Climate appears to have been key to the formation of the latitudinal diversity gradient, but the processes through which climate shaped species richness remain unclear. We tested predictions of the time for speciation, carrying capacity and diversification rate latitudinal diversity gradient hypotheses in a trans‐marine/freshwater clade of fishes. LocationGlobal in marine and freshwater environments. TaxonClupeiformes (anchovies, herrings, sardines and relatives). MethodsWe tested predictions of latitudinal diversity gradient hypotheses using a molecular phylogeny, species distribution data and phylogenetic comparative approaches. To test the time for speciation hypothesis, we conducted ancestral state reconstructions to infer the ages of temperate, subtropical and tropical lineages and frequency of evolutionary transitions between climates. We tested the carry capacity hypothesis by characterizing changes in net diversification rates through time. To test the diversification rate hypothesis, we qualitatively compared the diversification rates of temperate, subtropical and tropical lineages and conducted statistical tests for associations between latitude and diversification rates. ResultsWe identified four transitions to temperate climates and two transitions out of temperate climates. We found no differences in diversification rates among temperate and tropical clupeiforms. Net diversification rates remained positive in crown Clupeiformes since their origin ~150 Ma in both tropical and temperate lineages. Climate niche characters exhibited strong phylogenetic signal. All temperate clupeiform lineages arose <50 Ma, after the Early Eocene Climatic Optimum. Main conclusionsOur results support the time for speciation hypothesis, which proposes that climate niche conservatism and fluctuations in the extent of temperate climates limited the time for species to accumulate in temperate climates, resulting in the latitudinal diversity gradient. We found no support for the carrying capacity or diversification rate hypotheses. 

Abstract Evolutionary transitions between marine and freshwater ecosystems have occurred repeatedly throughout the phylogenetic history of fishes. The theory of ecological opportunity predicts that lineages that colonize species-poor regions will have greater potential for phenotypic diversification than lineages invading species-rich regions. Thus, transitions between marine and freshwaters may promote phenotypic diversification in trans-marine/freshwater fish clades. We used phylogenetic comparative methods to analyze body size data in nine major fish clades that have crossed the marine/freshwater boundary. We explored how habitat transitions, ecological opportunity, and community interactions influenced patterns of phenotypic diversity. Our analyses indicated that transitions between marine and freshwater habitats did not drive body size evolution, and there are few differences in body size between marine and freshwater lineages. We found that body size disparity in freshwater lineages is not correlated with the number of independent transitions to freshwaters. We found a positive correlation between body size disparity and overall species richness of a given area, and a negative correlation between body size disparity and diversity of closely related species. Our results indicate that the diversity of incumbent freshwater species does not restrict phenotypic diversification, but the diversity of closely related taxa can limit body size diversification. Ecological opportunity arising from colonization of novel habitats does not seem to have a major effect in the trajectory of body size evolution in trans-marine/freshwater clades. Moreover, competition with closely related taxa in freshwaters has a greater effect than competition with distantly related incumbent species.