Reeling in answers to the "freshwater fish paradox" - PNAS
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INNER WORKINGS
INNER WORKINGS
Reeling in answers to the “freshwater fish paradox”
Amy McDermott, Science Writer
Some 500 species of cichlid fish dart through the turbid and freshwater environments seems paradoxical—and in-
yellowish waters of East Africa’s Lake Victoria; little insec- deed, has been labeled the “freshwater fish paradox.”
tivores fin over the pebbles near shore, while larger Ichthyologists working in the 1970s first theorized that
predatory species cruise deeper water. Although the freshwater fish might evolve faster, driving up their rela-
oceans are the evocative epicenters of fish biodiversity tive diversity, because they live in geographically frag-
worldwide, freshwater streams, rivers, and lakes like mented tributaries with more opportunities for evolution
Victoria actually hold just as much fish diversity. Of by isolation than in continuous seas (3, 4).
the roughly 30,000 known fish species, about half live But new research by evolutionary biologist Eliz-
in freshwater (1). The longstanding question is why. abeth Miller, now a postdoc at the University of
Most biologists expect the vast oceans to be more Oklahoma in Norman, and others suggests there’s
diverse—as a general rule, larger areas tend to contain more nuance to the story. Rates of fish evolution in
more species (2). With some 97% of Earth’s water volume salt and freshwater may not be so different after all.
locked up in the sea, and just 0.0093% in habitable fresh- Some species, most prominently the fast-evolving
water, the even split of fish species richness between marine cichlids, may account for the perceived discrepancy.
The explosive adaptive radiation of cichlids—such as the colorful male and drab female of the species Lithochromis rufus
native to Lake Victoria—could help explain the comparable diversity of freshwater and saltwater fishes. Image credit:
Florian Moser (photographer).
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Published September 1, 2021.
PNAS 2021 Vol. 118 No. 36 e2113780118 https://doi.org/10.1073/pnas.2113780118 | 1 of 4
The bigger the area, the more species you should count.
Naturalists first made this observation in the 18th century,
for instance documenting that larger islands indeed had
more species than smaller ones (6, 7). Technically, it’s
not a true paradox— patterns of species richness don’t
contradict theory necessarily. “Nobody has ever sug-
gested a single type of species–area relationship across
all habitats,” says University of Oxford, UK, biogeogra-
pher Robert Whittaker. Oceans and rivers have different
relationships; the type of habitat matters, not just the
sheer size of the ecosystem in question.
The paradox label may not be quite right, but the
pattern is perplexing. Studies of the so-called paradox
are trying to explain this unusual pattern of species
richness, explains ichthyologist Peter Wainwright at
the University of California, Davis. “The real question
there,” he says, is “what exactly is the history of fishes
in these two habitats?” Angelfishes and butterflyfishes
Marine fish communities, such as this one in the Galapagos Islands featuring the waft through saltwater reefs, while cichlids swirl in
Ember parrotfish, Scarus rubroviolaceus, are famous for their diversity. But
freshwater African rift lakes, each as a result of their
researchers have long been unsure as to why freshwater fishes are just as species
rich as ocean fishes. Image credit: Ricardo Betancur (photographer). own evolutionary histories.
In 2012, evolutionary ecologist John J. Wiens at
Getting to the bottom of the freshwater fish par- the University of Arizona in Tucson coauthored one of
adox could shed light on a much larger question in the first studies tackling the apparent paradox (8). He
tested whether freshwater fish species had diversified
evolutionary biology: Why does species richness vary
faster than saltwater groups, one possible explanation
between different habitats in the first place? Across all
for the higher freshwater diversity per unit area. The
macroscopic organisms, about 80% of species are
study began with a phylogenetic tree of 97 ray-finned
terrestrial, 15% are marine, and 5% are freshwater (5).
fish families, representing 22 clades —the majority of
Understanding what’s going on in fish could help illu-
fish diversity—based on differences in one gene from
minate more general mechanisms at work in other an-
124 different fish species. For every clade, Wiens and
imals globally on land and sea. co-authors calculated diversification rates—speciation
rate minus extinction rate—using an estimator that is
The Paradox That Isn’t similar to taking the logarithm of the number of spe-
The freshwater fish paradox seems to contradict a core cies, divided by the age of the clade. Hence, a young
ecological principle known as the species–area relationship: clade with many species would have a high diversifi-
cation rate, while an old clade with only a few species
would have a low rate. Each of the 22 clades had ei-
ther freshwater species, saltwater species, or a mix of
freshwater and saltwater species.
It turned out that freshwater and saltwater clades
had similar diversification rates. A closer look at the
phylogenetic tree pointed to a possible reason: Two
of the largest, most diverse fish clades—the predominantly
freshwater Ostariophysi and the predominantly saltwater
Percomorpha—were roughly the same age, about 150
million years old, and diversifying at similar rates.
Although that work was state-of-the-art at the time,
says fish evolutionary biologist Ricardo Betancur at the
University of Oklahoma in Norman, studies since 2012
have used denser phylogenies, including thousands
more species and many more genes, and updated
statistical tools to make new inferences about fish
evolution. Yet there is still no consensus. Some newer
studies even suggest that marine lineages diversified
faster than freshwater groups; others come to the
exact opposite conclusion (9, 10).
Evolutionary biologist Ole Seehausen calls Neochromis simotes “one of the most
amazing species in the radiation.” The fish has highly adapted mouthparts—rows of Fishing for Answers
densely spaced and movably implanted teeth—that enable grazing algae on the
rocks in the rapids of the Nile, just after that river leaves Lake Victoria. The roughly 20
“We’re in a big mess of macroevolutionary results,”
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species in the Neochromis genus are all endemic to the lake, arising in the last 15,000 says evolutionary biologist Daniel Rabosky at the
years. Image Credit: Ole Seehausen (University of Bern, Bern, Switzerland). University of Michigan in Ann Arbor. Trying to make
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https://doi.org/10.1073/pnas.2113780118 Inner Workings: Reeling in answers to the “freshwater fish paradox”
inferences from imperfect data is one major reason fastest cases of adaptive radiation known in the animal
why. Diversification is speciation minus extinction. world (see Box). They all descend from several dis-
And although speciation rates are simple to calculate, tantly related species that came together and formed
based on the length and branching of a phylogenetic a hybrid population in the region in the last 150,000
tree, extinction rates are harder in part because the years. Indeed, in Lake Victoria, 500 new species
fossil record doesn’t preserve the vast majority of fish evolved in just the last 15,000 years (13). Miller real-
species, and in part because phylogenetic trees don’t ized that when cichlids had been lumped in with other
preserve any extinct species. It’s unclear when past freshwater fish in past analyses, the cichlids’ light
groups died out. speed diversification rates have skewed the results,
Nevertheless, existing diversification studies do making it appear that freshwater fish in general evolve
attempt to estimate extinction rates, sometimes arbi- faster than marine ones.
trarily, Rabosky says. “It’s taken us a decade to figure Miller herself had found elevated diversification
out just how nonrobust those estimates of extinction rates for freshwater members of the bony fish clade
are, and I don’t trust any of it,” he says. Percomorpha in a 2018 study (14). She repeated her
To explain patterns of fish species richness while analysis in a 2021 article, this time excluding cichlids.
avoiding the pitfalls of extinction calculations, Rabosky Sure enough, diversification rates for the remaining
authored a 2020 study analyzing the most robust fish freshwater and saltwater groups roughly matched (15).
tree of life to date. As part of a large collaboration, he Probing deeper, Miller classified the remaining fishes
and coauthors originally published the tree in 2018, as lake, river, or marine species and compared their
based on 11,638 fish species, 27 genes, and dated diversification rates across habitats. She found that
using 130 fossil calibrations. However, in 2020, Rabosky lake fish species in general do have higher diversifi-
limited the scope of his analysis to recent speciation cation rates than river or marine species. Lakes seem
rates in the last 50 million years, where confidence in to be crucibles of exceptionally fast evolution, of
the data is highest (11, 12). He knew that bursts of rapid which the cichlids are perhaps the most extreme ex-
species formation often accompany transitions to new ample, she says. Researchers aren’t yet sure why, but
habitats. If fish arose in the oceans but then invaded it’s possible that when lakes periodically fill, early
freshwater multiple times, perhaps they’d gone through colonists are released from predation or competition,
bursts of speciation that explain the relatively high di- so they’re free to quickly diversify into available
versity of freshwater fish per unit area today. niches. Looking ahead, future ecological fieldwork will
Rabosky used a model based on habitat data and need to test whether fish really do experience less
known relationships between fish lineages to scan the competition in lakes, she says. Another possibility is
phylogeny for large groups of extant freshwater fish in that fish have more stratified niches by depth in lakes
which all ancestors are marine. It identified the time and so can avoid competition by diving deeper,
point in the tree when those freshwater lineages di- compared with typically shallower rivers.
verged from their marine ancestors then compared But the rapid diversification of lake fish species
speciation rates in those groups before and after the only tells part of the story, as lake fishes are a minority
transition to freshwater. Unexpectedly, there was no of freshwater groups. Cichlids, for example, total only
evidence for a general trend of rapid speciation after about 2,500 of the 15,000 freshwater species (16).
colonizing new habitats. However, two huge groups Even without them, marine and freshwater habitats
did speciate faster upon entering freshwater: the would be similarly diverse. The vast majority of fresh-
cichlids and the Otophysi (minnows, catfishes, pira- water fish species evolved in rivers. When Miller
nhas, and a number of other groups), which together looked to river fish in her 2021 analysis, she found
represent about 80% of freshwater fish diversity. Per- diversification rates comparable with those of marine
haps something about these exceptional clades could groups. Miller also found that the major fish groups in
help explain patterns of freshwater species richness. rivers and oceans have been diversifying at similar
rates on average for much of their history, roughly the
Moving the Needle last 100 million years. She also repeated her analysis
When Elizabeth Miller read Rabosky’s 2020 work, a but calculated more-reliable speciation rates and, re-
lightbulb went on. The cichlids in Lake Victoria are the assuringly, found the same trends.
Cichlid Secrets
Cichlids speciate incredibly fast; recent work is offering good clues as to how they do it. The answer seems to be unusual genetic
flexibility, according to a 2020 study by evolutionary biologist Ole Seehausen at the University of Bern, in Switzerland. Seehausen and
his colleagues analyzed 100 Lake Victoria cichlid genomes, sampling species across habitats and niches. Using DNA extracted from
the preserved pectoral fins of each fish, the researchers compared and contrasted the genomes of cichlids from different dietary
groups and habitats (17).
They found hundreds of distinct DNA regions strongly tied to different ecological niches and scattered across 22 chromosomes.
“We think that’s the key to make hundreds of species and not just two or three,” Seehausen says. When the fish hybridize, they can
rearrange these modular genes, “almost like Lego bricks,” he says, to build many possible combinations suited, for example, to a
rocky inshore fish that feeds on insects, or one that eats the same bugs but lives in weedy lake grass.
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Inner Workings: Reeling in answers to the “freshwater fish paradox” https://doi.org/10.1073/pnas.2113780118The latest findings hint that, more than anything not necessary to explain high richness in freshwater.
else, the so-called paradox is driven by the age of These latest studies suggest that “there [are] a lot of
certain fish groups and how long they’ve been diver- ways to end up with a lot of species,” Miller says.
sifying at similar rates, as Wiens suggested in 2012. Rapid evolution in lakes is one way. Slower and
Miller, who worked with him on her PhD, found in her steadier evolution in rivers and oceans is another.
latest work that modern marine and riverine fish spe- Clearly, fish species do not obey the same rules
cies, in particular, have been accumulating diversity at across habitats.
comparable rates for 100 million years. Although her Taken together, these findings suggest that per-
study is not the first to offer an explanation based on haps evolutionary biologists should revisit the way
similar ages and similar diversification rates, that ex- they think about differences in species richness across
planation was largely overlooked in the last decade in habitats. There is a long tradition of efforts to explain
favor of the focus on contrasting diversification rates, biodiversity gradients globally, not just for fish but for
Miller notes. terrestrial, marine, and freshwater animals and plants.
Since the earliest days of the so-called paradox, Biologists and ecologists typically invoke different
ichthyologists have hypothesized that fish must di- rates of speciation and diversification to explain
versify faster in freshwater because freshwater systems differences in species richness at large. Maybe the
are so fragmented compared with the oceans. Fish lesson from fish, Miller points out, is that the answer
populations separated into isolated pockets this way doesn’t have to be different rates of speciation
would in theory have more opportunities for diversi- and extinction at all. The contribution of outliers
fication. Miller’s findings suggest that 100 million could be masking the actual history of evolution in
years is long enough; faster speciation, she writes, is many groups.
1 O. Seehausen, C. E. Wagner, Speciation in freshwater fishes. Annual Reviews 45, 621–651 (2014).
2 R. M. May, Biological diversity: Differences between land and sea. Phil. Trans. Royal. Soc. B. 343, 105–111 (1994).
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6 T. J. Matthews, K. A. Triantis, R. J. Whittaker, Eds., The Species-Area Relationship (Cambridge University Press, Cambridge, 2021).
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Ecological Society of America, Contributions, 10.1890/0012-9623-91.3.294 (2010).
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12 D. L. Rabosky, Speciation rate and the diversity of fishes in freshwaters and the oceans. J. Biogeogr. 47, 1207–1217 (2020).
13 J. I. Meier et al., Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nat. Commun. 8, 14363 (2017).
14 E. C. Miller, K. T. Hayashi, D. Song, J. J. Wiens, Explaining the ocean’s richest biodiversity hotspot and global patterns of fish diversity.
Proc. Biol. Sci. 285, 20181314 (2018).
15 E. C. Miller, Comparing diversification rates in lakes, rivers, and the sea. Evolution 10.1111/evo.14295. (2021).
16 P. D. Danley et al., The impact of the geologic history and paleoclimate on the diversification of East African cichlids. Int. J. Evol. Biol.
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