An official website of the United States government
Synopsis Understanding the processes that shaped the distribution of species richness across the Tree of Life is a central macroevolutionary research agenda. Major ecological innovations, including transitions between habitats, may help to explain the striking asymmetries of diversity that are often observed between sister clades. Here, we test the impact of such transitions on speciation rates across decapod crustaceans, modeling diversification dynamics within a phylogenetic framework. Our results show that, while terrestrial lineages have higher speciation rates than either marine or freshwater lineages, there is no difference between mean speciation rates in marine and freshwater lineages across Decapoda. Partitioning our data by infraorder reveals that those clades with habitat heterogeneity have higher speciation rates in freshwater and terrestrial lineages, with freshwater rates up to 1.5 times faster than marine rates, and terrestrial rates approximately four times faster. This averaging out of marine and freshwater speciation rates results from the varying contributions of different clades to average speciation rates. However, with the exception of Caridea, we find no evidence for any causal relationship between habitat and speciation rate. Our results demonstrate that while statistical generalizations about ecological traits and evolutionary rates are valuable, there are many exceptions. Hence, while freshwater and terrestrial lineages typically speciate faster than their marine relatives, there are many atypically slow freshwater lineages and fast marine lineages across Decapoda. Future work on diversification patterns will benefit from the inclusion of fossil data, as well as additional ecological factors.
more »
« less
Patterns of Phenotypic Evolution Associated with Marine/Freshwater Transitions in Fishes
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.
more »
« less
- Award ID(s):
- 2135085
- PAR ID:
- 10370152
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative And Comparative Biology
- Volume:
- 62
- Issue:
- 2
- ISSN:
- 1540-7063
- Format(s):
- Medium: X Size: p. 406-423
- Size(s):
- p. 406-423
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Habitat transitions are key potential explanations for why some lineages have diversified and others have not—from Anolis lizards to Darwin's finches. The ecological ramifications of marine-to-freshwater transitions for fishes suggest evolutionary contingency: some lineages maintain their ancestral niches in novel habitats (niche conservatism), whereas others alter their ecological role. However, few studies have considered phenotypic, ecological, and lineage diversification concurrently to explore this issue. Here, we investigated the macroevolutionary history of the taxonomically and ecologically diverse Neotropical freshwater river rays (subfamily Potamotrygoninae), which invaded and diversified in the Amazon and other South American rivers during the late Oligocene to early Miocene. We generated a time-calibrated, multi-gene phylogeny for Potamotrygoninae and reconstructed evolutionary patterns of diet specialization. We measured functional morphological traits relevant for feeding and used comparative phylogenetic methods to examine how feeding morphology diversified over time. Potamotrygonine trophic and phenotypic diversity are evenly partitioned (non-overlapping) among internal clades for most of their history, until 20–16 mya, when more recent diversification suggests increasing overlap among phenotypes. Specialized piscivores (Heliotrygon and Paratrygon) evolved early in the history of freshwater stingrays, while later trophic specialization (molluscivory, insectivory, and crustacivory) evolved in the genus Potamotrygon. Potamotrygonins demonstrate ecological niche lability in diets and feeding apparatus; however, diversification has mostly been a gradual process through time. We suggest that competition is unlikely to have limited the potamotrygonine invasion and diversification in South America.more » « less
-
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.more » « less
-
ABSTRACT Colonization of a novel habitat is often followed by radiation in the wake of ecological opportunity. Alternatively, some habitats should be inherently more constraining than others if the challenges of that environment have few evolutionary solutions. We examined the push-and-pull of these factors on evolution following habitat transitions, using anglerfishes (Lophiiformes) as a model. Deep-sea fishes are notoriously difficult to study, and poor sampling has limited progress thus far. Here we present a new phylogeny of anglerfishes with unprecedented taxonomic sampling (1,092 loci and 40% of species), combined with three-dimensional phenotypic data from museum specimens obtained with micro-CT scanning. We use these datasets to examine the tempo and mode of phenotypic and lineage diversification using phylogenetic comparative methods, comparing lineages in shallow and deep benthic versus bathypelagic habitats. Our results show that anglerfishes represent a surprising case where the bathypelagic lineage has greater taxonomic and phenotypic diversity than coastal benthic relatives. This defies expectations based on ecological principles since the bathypelagic zone is the most homogeneous habitat on Earth. Deep-sea anglerfishes experienced rapid lineage diversification concomitant with colonization of the bathypelagic zone from a continental slope ancestor. They display the highest body, skull and jaw shape disparity across lophiiforms. In contrast, reef-associated taxa show strong constraints on shape and low evolutionary rates, contradicting patterns suggested by other shallow marine fishes. We found that Lophiiformes as a whole evolved under an early burst model with subclades occupying distinct body shapes. We further discuss to what extent the bathypelagic clade is a secondary adaptive radiation, or if its diversity can be explained by non-adaptive processes.more » « less
-
Synopsis Evolutionary transitions between habitats have been catalysts for some of the most stunning examples of adaptive diversification, with novel niches and new resources providing ecological opportunity for such radiations. In aquatic animals, transitions from saltwater to freshwater habitats are rare, but occur often enough that in the Neotropics for example, marine-derived fishes contribute noticeably to regional ichthyofaunal diversity. Here, we investigate how morphology has evolved in a group of temperate fishes that contain a marine to freshwater transition: the sculpins (Percomorpha; Cottoidea). We devised a novel method for classifying dietary niche and relating functional aspects of prey to their predators. Coupled with functional measurements of the jaw apparatus in cottoids, we explored whether freshwater sculpins have fundamentally changed their niche after invading freshwater (niche lability) or if they retain a niche similar to their marine cousins (niche conservatism). Freshwater sculpins exhibit both phylogeographical and ecological signals of phylogenetic niche conservatism, meaning that regardless of habitat, sculpins fill similar niche roles in either saltwater or freshwater. Rather than competition guiding niche conservatism in freshwater cottoids, we argue that strong intrinsic constraints on morphological and ecological evolution are at play, contra to other studies of diversification in marine-derived freshwater fishes. However, several intertidal and subtidal sculpins as well as several pelagic freshwater species from Lake Baikal show remarkable departures from the typical sculpin bauplan. Our method of prey categorization provides an explicit, quantitative means of classifying dietary niche for macroevolutionary studies, rather than relying on somewhat arbitrary means used in previous literature.more » « less
