Phylogenomics, Lineage Diversification Rates, and the Evolution of Diadromy in Clupeiformes (Anchovies, Herrings, Sardines, and Relatives).

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 longstanding 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 among some populations, increasing the likelihood of speciation in diadromous lineages relative to non-diadromous 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 (non-stationarity) 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 thirteen transitions to diadromy, all during the Cenozoic Era (ten origins of anadromy, two origins of catadromy, and one origin of amphidromy), and seven losses of diadromy. Two diadromous lineages rapidly generated non-diadromous 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 non-diadromous 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.

Diadromy Drives Elevated Rates of Trait Evolution and Ecomorphological Convergence in Clupeiformes (Herring, Shad, and Anchovies).

AbstractMigration can have a profound influence on rates and patterns of phenotypic evolution. Diadromy is the migration between marine and freshwater habitats for feeding and reproduction that can require individuals to travel tens to thousands of kilometers. The high energetic demands of diadromy are predicted to select for ecomorphological traits that maximize swimming and locomotor efficiency. Intraspecific studies have shown repeated instances of divergence among diadromous and nondiadromous populations in locomotor and foraging traits, which suggests that at a macroevolutionary scale diadromous lineages may experience convergent evolution onto one or multiple adaptive optima. We tested for differences in rates and patterns of phenotypic evolution among diadromous and nondiadromous lineages in Clupeiformes, a clade that has evolved diadromy more than 10 times. Our results show that diadromous clupeiforms show convergent evolution for some locomotor traits and faster rates of evolution, which we propose are adaptive responses to the locomotor demands of migration. We also find evidence that diadromous lineages show convergence into multiple regions of multivariate trait space and suggest that these respective trait spaces are associated with differences in migration and trophic ecology. However, not all locomotor traits and no trophic traits show evidence of convergence or elevated rates of evolution associated with diadromy. Our results show that long-distance migration influences the tempo and patterns of phenotypic evolution at macroevolutionary scales, but there is not a single diadromous syndrome.

Whole genome resequencing identifies local adaptation associated with environmental variation for redband trout.

Aquatic ectotherms are predicted to harbour genomic signals of local adaptation resulting from selective pressures driven by the strong influence of climate conditions on body temperature. We investigated local adaptation in redband trout (Oncorhynchus mykiss gairdneri) using genome scans for 547 samples from 11 populations across a wide range of habitats and thermal gradients in the interior Columbia River. We estimated allele frequencies for millions of single nucleotide polymorphism loci (SNPs) across populations using low-coverage whole genome resequencing, and used population structure outlier analyses to identify genomic regions under divergent selection between populations. Twelve genomic regions showed signatures of local adaptation, including two regions associated with genes known to influence migration and developmental timing in salmonids (GREB1L, ROCK1, SIX6). Genotype-environment association analyses indicated that diurnal temperature variation was a strong driver of local adaptation, with signatures of selection driven primarily by divergence of two populations in the northern extreme of the subspecies range. We also found evidence for adaptive differences between high-elevation desert vs. montane habitats at a smaller geographical scale. Finally, we estimated vulnerability of redband trout to future climate change using ecological niche modelling and genetic offset analyses under two climate change scenarios. These analyses predicted substantial habitat loss and strong genetic shifts necessary for adaptation to future habitats, with the greatest vulnerability predicted for high-elevation desert populations. Our results provide new insight into the complexity of local adaptation in salmonids, and important predictions regarding future responses of redband trout to climate change.

Patterns of Body Shape Diversity and Evolution in Intertidal and Subtidal Lineages of Combtooth Blennies (Blenniidae).

Marine intertidal zones can be harsher and more dynamic than bordering subtidal zones, with extreme and temporally variable turbulence, water velocity, salinity, temperature, and dissolved oxygen levels. Contrasting environmental conditions and ecological opportunities in subtidal versus intertidal habitats may generate differing patterns of morphological diversity. In this study we used phylogenetic comparative methods, measurements of body length, and two-dimensional landmarks to characterize body shape and size diversity in combtooth blennies (Ovalentaria: Blenniidae) and test for differences in morphological diversity between intertidal, subtidal, and supralittoral zones. We found that subtidal combtooth blennies have significantly higher body shape disparity and occupy a region of morphospace three times larger than intertidal lineages. The intertidal morphospace was almost entirely contained within the subtidal morphospace, showing that intertidal combtooth blennies did not evolve unique body shapes. We found no significant differences in body size disparity between tidal zones, no correlations between body shape and tidal zone or body size and tidal zone, and no body shape convergence associated with tidal zone. Our findings suggest that a subset of combtooth blenny body shapes are suitable for life in both subtidal and intertidal habitats. Many species in regions of morphospace unique to subtidal combtooth blennies exhibit distinct microhabitat use, which suggests subtidal environments promoted morphological diversification via evolutionary microhabitat transitions. In contrast, limited intertidal body shape diversity may be due to strong selective pressures that constrained body shape evolution and environmental filtering that prevented colonization of intertidal zones by certain subtidal body shapes.

Taillessness and skeletal deformity in striped piggy Pomadasys stridens (Osteichthyes: Haemulidae) from the Persian Gulf.

Taillessness (absence of the caudal fin and some of the caudal peduncle) and skeletal deformity is described in 2 striped piggy Pomadasys stridens (Haemulidae) specimens collected from the Persian Gulf along the coast of Hormuz Island, Iran. Deformed specimens were entirely missing caudal fins along with at least 1 caudal vertebra, caudal portions of vertebral columns were bent dorsoventrally, posterior sections of swim bladders were reduced in size, and caudal vertebral centra were compacted anteroposteriorly in 1 individual. Environmental conditions in the Persian Gulf may be responsible for these deformities, but genetic causes cannot be entirely ruled out.

Systematics of the combtooth blenny clade Omobranchus (Blenniidae: Omobranchini), with notes on early life history stages.

The combtooth blenny (Blenniidae) genus Omobranchus contains small, cryptobenthic fishes common to nearshore habitats throughout the Indo-West Pacific. Recent molecular systematic studies have resolved Omobranchus as monophyletic but little research has been done to resolve species-level relationships. Herein, phylogenetic analyses of one mitochondrial (CO1) and four nuclear (ENC1, myh6, sreb2, and tbr1) genes provide evidence for the monophyly of Omobranchus and support for the elongatus and banditus species group. Sampling of multiple individuals from widespread species (O. ferox, O. punctatus, and O. elongatus) suggested that the Thai-Malay Peninsula is a phylogeographic break that may be a historic barrier to gene flow. Additionally, common meristics and other morphological characters are used to describe an early life history stage of O. ferox and O. punctatus.

Phylogenetic analysis of trophic niche evolution reveals a latitudinal herbivory gradient in Clupeoidei (herrings, anchovies, and allies).

Biotic and abiotic forces govern the evolution of trophic niches, which profoundly impact ecological and evolutionary processes and aspects of species biology. Herbivory is a particularly interesting trophic niche because there are theorized trade-offs associated with diets comprised of low quality food that might prevent the evolution of herbivory in certain environments. Herbivory has also been identified as a potential evolutionary "dead-end" that hinders subsequent trophic diversification. For this study we investigated trophic niche evolution in Clupeoidei (anchovies, sardines, herrings, and their relatives) and tested the hypotheses that herbivory is negatively correlated with salinity and latitude using a novel, time-calibrated molecular phylogeny, trophic guilds delimited using diet data and cluster analysis, and standard and phylogenetically-informed statistical methods. We identified eight clupeoid trophic guilds: molluscivore, terrestrial invertivore, phytoplanktivore, macroalgivore, detritivore, piscivore, crustacivore, and zooplanktivore. Standard statistical methods found a significant negative correlation between latitude and the proportion of herbivorous clupeoids (herbivorous clupeoid species/total clupeoid species), but no significant difference in the proportion of herbivorous clupeoids between freshwater and marine environments. Phylogenetic least squares regression did not identify significant negative correlations between latitude and herbivory or salinity and herbivory. In clupeoids there were five evolutionary transitions from non-herbivore to herbivore guilds and no transitions from herbivore to non-herbivore guilds. There were no transitions to zooplanktivore, the most common guild, but it gave rise to all trophic guilds, except algivore, at least once. Transitions to herbivory comprised a significantly greater proportion of diet transitions in tropical and subtropical (<35°) relative to temperate areas (>35°). Our findings suggest cold temperatures may constrain the evolution of herbivory and that herbivory might act as an evolutionary "dead-end" that hinders subsequent trophic diversification, while zooplanktivory acts as an evolutionary "cradle" that facilitates trophic diversification.

Systematics of Clupeiformes and testing for ecological limits on species richness in a trans-marine/freshwater clade

Clupeiformes (herring, sardines, shad, anchovies and allies) are a globally distributed clade with nearly 400 marine, freshwater, and diadromous species. Although best known as filter feeding fishes that form large schools, this group occupies a diverse array of trophic guilds and habitats. Theory suggests that species richness in clades is modulated by ecological limits, which results in diversity-dependent clade growth, a pattern that most clades exhibit. As a trans-marine/freshwater clade that has undergone repeated transitions between marine and freshwaters, Clupeiformes are an excellent system for investigating the interplay between ecological diversity and macroevolutionary dynamics. In this study we review the systematics of Clupeiformes and explore discordance in phylogenetic relationships and divergence times between mitochondrial and nuclear loci. We then use comparative methods to test whether ecological limits regulate diversity in Clupeiformes. We find discordance in phylogenetic relationships at various taxonomic scales, but also considerable agreement between genomes. Our results suggest that trans-marine/freshwater clades are able to circumvent ecological limits on clade growth at regional, but not on local scales. Our study demonstrates that phylogenies are a critical link between ecology and macroevolutionary dynamics, and suggests habitat transitions can play a key role in shaping diversity patterns, particularly in the neotropics.(AU)

Clupeiformes (apapás, sardinhas e manjubas) são um clado globalmente distribuído com quase 400 espécies marinhas, de água doce e diádromas. Embora mais conhecida pela presença de peixes filtradores formadores de cardumes, este grupo apresenta uma diversidade de guilda e habitats tróficos. A teoria sugere que a riqueza de espécies em clados é modulada por limites ecológicos, o que resulta em um crescimento dependente da diversidade, um padrão que a maioria dos clados exibem. Como um clado que sofreu repetidas transições entre águas marinhas e as águas doces, os clupeiformes são um excelente grupo para investigar a interação entre a diversidade ecológica e a dinâmica macroevolutiva. Neste estudo, revisamos a sistemática de Clupeiformes e exploramos a discordância nas relações filogenéticas e os tempos de divergência entre loci mitocondriais e nucleares. Em seguida, utilizamos métodos comparativos para testar se os limites ecológicos regulam a diversidade em Clupeiformes. Encontramos discordância nas relações filogenéticas em várias escalas taxonômicas, mas também considerável concordância entre os genomas. Nossos resultados sugerem que clados que sofreram sucessivas transições entre águas marinhas e águas doces são capazes de contornar os limites ecológicos do crescimento durante a sua diversificação em escala global, mas não localmente. Nosso estudo demonstra que as filogenias apresentam um vínculo crítico entre a ecologia e a dinâmica macroevolutiva, e sugere que as transições de hábitats podem desempenhar um papel fundamental na modelagem dos padrões de diversidade, particularmente no neotrópico.(AU)