Alternating regimes of shallow and deep-sea diversification explain a species-richness paradox in marine fishes.

The deep sea contains a surprising diversity of life, including iconic fish groups such as anglerfishes and lanternfishes. Still, >65% of marine teleost fish species are restricted to the photic zone <200 m, which comprises less than 10% of the ocean's total volume. From a macroevolutionary perspective, this paradox may be explained by three hypotheses: 1) shallow water lineages have had more time to diversify than deep-sea lineages, 2) shallow water lineages have faster rates of speciation than deep-sea lineages, or 3) shallow-to-deep sea transition rates limit deep-sea richness. Here we use phylogenetic comparative methods to test among these three non-mutually exclusive hypotheses. While we found support for all hypotheses, the disparity in species richness is better described as the uneven outcome of alternating phases that favored shallow or deep diversification over the past 200 million y. Shallow marine teleosts became incredibly diverse 100 million y ago during a period of warm temperatures and high sea level, suggesting the importance of reefs and epicontinental settings. Conversely, deep-sea colonization and speciation was favored during brief episodes when cooling temperatures increased the efficiency of the ocean's carbon pump. Finally, time-variable ecological filters limited shallow-to-deep colonization for much of teleost history, which helped maintain higher shallow richness. A pelagic lifestyle and large jaws were associated with early deep-sea colonists, while a demersal lifestyle and a tapered body plan were typical of later colonists. Therefore, we also suggest that some hallmark characteristics of deep-sea fishes evolved prior to colonizing the deep sea.

Many ways to build an angler: diversity of feeding morphologies in a deep-sea evolutionary radiation.

Almost nothing is known about the diets of bathypelagic fishes, but functional morphology can provide useful tools to infer ecology. Here we quantify variation in jaw and tooth morphologies across anglerfishes (Lophiiformes), a clade spanning shallow and deep-sea habitats. Deep-sea ceratioid anglerfishes are considered dietary generalists due to the necessity of opportunistic feeding in the food-limited bathypelagic zone. We found unexpected diversity in the trophic morphologies of ceratioid anglerfishes. Ceratioid jaws span a functional continuum ranging from species with numerous stout teeth, a relatively slow but forceful bite, and high jaw protrusibility at one end (characteristics shared with benthic anglerfishes) to species with long fang-like teeth, a fast but weak bite and low jaw protrusibility at the other end (including a unique 'wolftrap' phenotype). Our finding of high morphological diversity seems to be at odds with ecological generality, reminiscent of Liem's paradox (morphological specialization allowing organisms to have broader niches). Another possible explanation is that diverse ceratioid functional morphologies may yield similar trophic success (many-to-one mapping of morphology to diet), allowing diversity to arise through neutral evolutionary processes. Our results highlight that there are many ways to be a successful predator in the deep sea.

Sexual Dichromatism Is Decoupled from Diversification over Deep Time in Fishes.

AbstractSexually selected traits have long been thought to drive diversification, but support for this hypothesis has been persistently controversial. In fishes, sexually dimorphic coloration is associated with assortative mating and speciation among closely related species, as shown in classic studies. However, it is unclear whether these results can generalize to explain diversity patterns across ray-finned fishes, which contain the majority of vertebrate species and 96% of fishes. Here, we use phylogenetic approaches to test for an association between sexual dichromatism and diversification rates (speciation minus extinction) in ray-finned fishes. We assembled dichromatism data for 10,898 species, a data set of unprecedented size. We found no difference in diversification rates between monochromatic and dichromatic species when including all ray-finned fishes. However, at lower phylogenetic scales (within orders and families), some intermediate-sized clades did show an effect of dichromatism on diversification. Surprisingly, dichromatism could significantly increase or decrease diversification rates. Moreover, we found no effect in many of the clades initially used to link dichromatism to speciation in fishes (e.g., cichlids) or an effect only at shallow scales (within subclades). Overall, we show how the effects of dichromatism on diversification are highly variable in direction and restricted to certain clades and phylogenetic scales.

Explaining the ocean's richest biodiversity hotspot and global patterns of fish diversity.

For most marine organisms, species richness peaks in the Central Indo-Pacific region and declines longitudinally, a striking pattern that remains poorly understood. Here, we used phylogenetic approaches to address the causes of richness patterns among global marine regions, comparing the relative importance of colonization time, number of colonization events, and diversification rates (speciation minus extinction). We estimated regional richness using distributional data for almost all percomorph fishes (17 435 species total, including approximately 72% of all marine fishes and approximately 33% of all freshwater fishes). The high diversity of the Central Indo-Pacific was explained by its colonization by many lineages 5.3-34 million years ago. These relatively old colonizations allowed more time for richness to build up through in situ diversification compared to other warm-marine regions. Surprisingly, diversification rates were decoupled from marine richness patterns, with clades in low-richness cold-marine habitats having the highest rates. Unlike marine richness, freshwater diversity was largely derived from a few ancient colonizations, coupled with high diversification rates. Our results are congruent with the geological history of the marine tropics, and thus may apply to many other organisms. Beyond marine biogeography, we add to the growing number of cases where colonization and time-for-speciation explain large-scale richness patterns instead of diversification rates.

Improved resolution and a novel phylogeny for the Neotropical triplefin blennies (Teleostei: Tripterygiidae).

The triplefin blennies (Teleostei: Tripterygiidae) are a diverse group of small-bodied benthic fishes associated with rocky or coral reefs. The Neotropics contain four genera and 26 species, many of which have only been recently described. A recent molecular phylogeny (Lin and Hastings, 2013) contrasts with previous phylogenies based on morphology in recovering the four Neotropical genera as a single clade with respect to the Indo-Pacific genera; however, relationships within and among genera were poorly resolved. This study reports a novel topology based on an expanded seven-loci molecular dataset. Individual gene trees have poor resolution, but concatenated analyses show strong support for most nodes, likely due to emergent support from concatenation. Consistent with Lin and Hastings (2013), three of the Neotropical genera, Axoclinus, Enneanectes, and Crocodilichthys, form a well-supported clade, but relationships of the fourth (Lepidonectes) are not confidently resolved. The monophyly of Axoclinus is well supported, but Enneanectes is paraphyletic with the inclusion of Axoclinus and Crocodilichthys. Improved resolution allows for reinterpretation of the biogeography of the Neotropical Tripterygiidae. Broader taxon sampling is still necessary for resolving the relationships within Tripterygiidae globally.

Historical biogeography supports Point Conception as the site of turnover between temperate East Pacific ichthyofaunas.

The cold temperate and subtropical marine faunas of the Northeastern Pacific meet within California as part of one of the few eastern boundary upwelling ecosystems in the world. Traditionally, it is believed that Point Conception is the precise site of turnover between these two faunas due to sharp changes in oceanographic conditions. However, evidence from intraspecific phylogeography and species range terminals do not support this view, finding stronger biogeographic breaks elsewhere along the coast. Here I develop a new application of historical biogeographic approaches to uncover sites of transition between faunas without needing an a priori hypothesis of where these occur. I used this approach to determine whether the point of transition between northern and southern temperate faunas occurs at Point Conception or elsewhere within California. I also examined expert-vetted latitudinal range data of California fish species from the 1970s and the 2020s to assess how biogeography could change with the backdrop of climate change. The site of turnover was found to occur near Point Conception, in concordance with the traditional view. I suggest that recent species- and population-level processes could be expected to give signals of different events from historical biogeography, possibly explaining the discrepancy across studies. Species richness of California has increased since the 1970s, mostly due to species's ranges expanding northward from Baja California (Mexico). Range shifts under warming conditions seem to be increasing the disparity between northern and southern faunas of California, creating a more divergent biogeography.

Comparing diversification rates in lakes, rivers, and the sea.

The diversity of species inhabiting freshwater relative to marine habitats is striking, given that freshwater habitats encompass <1% of Earth's water. The most commonly proposed explanation for this pattern is that freshwater habitats are more fragmented than marine habitats, allowing more opportunities for allopatric speciation and thus increased diversification rates in freshwater. However, speciation may be generally faster in sympatry than in allopatry, as illustrated by lacustrine radiations such as African cichlids. Such differences between rivers and lakes may be important to consider when comparing diversification broadly among freshwater and marine groups. Here I compared diversification rates of teleost fishes in marine, riverine and lacustrine habitats. I found that lakes had faster speciation and net diversification rates than other aquatic habitats. However, most freshwater diversity arose in rivers. Surprisingly, riverine and marine habitats had similar rates of net diversification on average. Biogeographic models suggest that lacustrine habitats are evolutionarily unstable, explaining the dearth of lacustrine species in spite of their rapid diversification. Collectively, these results suggest that strong diversification rate differences are unlikely to explain the freshwater paradox. Instead, this pattern may be attributable to the comparable amount of time spent in riverine and marine habitats over the 200-million-year history of teleosts.

Digest: Hypothesis testing in biogeography using phylogenetic trees.

How can we test whether biogeographic dispersal rates coincide with geologic events? Hua and Bromham developed a model-based approach to generate a null distribution of colonization times under constant dispersal rates, overcoming a problem related to the geometry of phylogenetic trees.