Art Courtesy of Alondra Moreno Santana.
In the depths of the midnight zone, where sunlight fails to penetrate and water pressure exceeds extremes, anglerfish have discovered an ocean of rich opportunity. This species has evolved to thrive over sixteen thousand feet below sea level, while exhibiting one of the highest levels of species diversity found in this ecosystem. In a recent study published in Current Biology, researchers in the lab of Thomas J. Near, a professor and chair of the Yale Department of Ecology and Evolutionary Biology, collaborated with the Dornburg Laboratory at UNC Charlotte to investigate the origins of the anglerfish’s rapid spread across the ocean and explore how the species flourished in such harsh conditions.
Periods of extreme environmental change can radically alter ecosystems and create new ecological opportunities that species may rapidly exploit. The evolution of new traits from a common ancestor, allowing species to adapt to different ecological roles, is known as adaptive radiation. Over time, adaptive radiation induces the development of many new species from a single common ancestor, forming a single clade. Fifty million years ago, the common ancestor of the anglerfish inhabited the ocean floor, also known as the benthic zone. This ancestor species was well-suited to “walk” across the ocean floor on modified fins. Based on their phylogenetic data on evolutionary relationships among species, the researchers hypothesized that this single ancestor gave rise to over two hundred species of anglerfish, many of whom now inhabit the deep open ocean. Anglerfish in the clade Ceratioidei are no longer confined to the ocean floor and exhibit a remarkable range of anatomical and physiological characteristics.
Chase Brownstein (YC ’23), a graduate student in Yale’s Department of Ecology and Evolutionary Biology, wanted to use his evolutionary expertise to understand the factors driving this incredible example of species diversification. Examining the phylogenetic evidence, Brownstein and his fellow researchers hypothesized that something external was driving this swift adaptive radiation: an intense environmental change might have pushed anglerfish into the midnight zone and, in the process, inspired a surprising new mating tactic.
It’s Gettin’ Hot in Here…
Climate change has impacted our planet for millions of years. One of Earth’s most notable climate change events coincided with the rise of the anglerfish. “What we’re inferring about the timing of diversification of deep-sea lineage is that it corresponds to global as well as oceanic temperatures,” said Near, the senior author of the paper.
During the Paleocene-Eocene Thermal Maximum (PETM), roughly fifty million years ago, a rapid increase in atmospheric pressures catalyzed a series of mass extinctions. Although anglerfish dwelled near the deepest depths of the ocean, even they weren’t safe from the incredible impacts of global warming.
The ancestors of the anglerfish were floor-dwelling scavengers that had modified, feet-like fins. However, as water temperatures increased during the PETM, food became a scarce resource for all marine life. The anglerfish thus left the ocean floor, losing their “feet” in the process. The anglerfishes’ express trip off the ocean floor prompted a cascade of adaptation. One could say that the anglerfishes’ ancestors walked so that the modern day fish could swim.
While the anglerfish had more feeding opportunities, they now found themselves with a new problem: reproduction. This led to the evolution of a unique adaptation—the fusion of males to females—which we observe in modern ceratioid anglerfishes. In this case, temperature change resulted in both the adaptation towards new habitats and the development of new reproductive modes that had not yet been seen.
’Til Death Do Us Part
An ancient warming of the oceans may have propelled the anglerfish into a new environment, but that’s just the beginning of the ceratioids’ evolutionary tale. In the isolation of this dark, new expanse, the only way to secure a partner for life meant never leaving each other’s side—literally. Enter sexual parasitism, a phenomenon that researchers believe was the catalyst for the rapid expansion of anglerfish into the midnight zone.
“We think that some form [of sexual parasitism] actually evolved right at the base, or right at the common ancestor […] of all living deep-sea ceratioid anglerfishes,” Brownstein said. If commitment were the only factor, Ceratioidei would be considered one of the best spouses of all time.
This parasitism can be temporary, permanent, or a combination of both. In most cases, the comparatively smaller male anglerfish will locate a female and attach himself to her. If this attachment becomes permanent, the male fuses with the female, integrating with her body as a sperm-producing organ. In the harsh conditions of the midnight zone, sexual parasitism has proven to be an iron-clad strategy for reproduction, sustaining the clade Ceratioidei and ensuring an opportunity for continued survival.
Fishing for Phylogenies
When did anglerfish adopt this reproductive tactic? Genome sequencing has been a key part of understanding the evolution of sexual dimorphism—major physical differences in sexes—as well as the reproductive modes of anglerfish. Previous studies relied solely on mitochondrial DNA or small samples of ten to twenty common genes, limiting their ability to trace the millions of years of evolutionary changes among anglerfish species. This study took over 1,300 genes from the more comprehensive modern-day nuclear genome and analyzed the mutations, achieving a newfound clarity that far surpasses past techniques.
By searching through these genomes, the researchers have determined that temporary attachment was likely the trait of the most recent common ancestor of all modern-day anglerfishes. This conclusion does not come without limitations as there are certain accepted biases in the data and remaining ambiguities in the evolutionary tree. As a result, reconstructing the exact timeline of when key traits evolved can be challenging. “We cannot do experiments that prove chickens are dinosaurs. We have to make inferences by reconstruction from the past,” Near said. Despite these limitations, the data indicate that sexual parasitism evolved at the start of the species’ move into the midnight zone, likely catalyzing the rapid expansion of ceratioid anglerfishes that followed. These new insights offer a clearer understanding of how anglerfish adapted to survive in such a harsh, low-density environment and reveal the evolutionary pressures that shaped their unique biology and behaviors.
Knock, Knock, Who’s There? — Not the Male
In order for sexual parasitism to work, a complex series of underlying genetic alterations have to occur. A key aspect of species survival is the ability to fend off foreign invaders like viruses and bacteria that find their way into an organism’s body. To enable male anglerfish to seamlessly attach to a female “host,” the adaptive immune systems of both the male and the female must be suppressed. Otherwise, each organism would mount an immune response against the other. While the stronger individual might survive, the infeasibility of mating would ultimately spell extinction for the species.
The researchers analyzed previously sequenced anglerfish genomes and identified genes related to the process of adaptive immunity, which targets specific pathogens. Their temporal analysis suggested that the deterioration of these genes aligned with the advent of sexual parasitism in Ceratioidei species. Sexual parasitism was the peanut butter, and the degeneration of adaptive immunity was the jelly; together, the two allowed for the reproductive success of anglerfishes in the midnight zone.
The devolution of adaptive immunity and the unique form of sexual reproduction employed by many members of Ceratioidei might have gotten the fish into the midnight zone, but that was just one part of their species diversification. Ceratioidei is an incredibly diverse clade, exhibiting traits from spikes to antennae to giant teeth. The sheer range of incredible adaptations among these species is shaped by the unique niches of the deep ocean, with the advent of sexual parasitism as a vessel for this journey.
Investigating the Gray Area
Reconstructing genetic histories is not a flawless science, and different approaches often lead to different results. This uncertainty creates “anomaly zones” in phylogenetic trees—the ecologist’s rendition of an extended family tree—where researchers are unable to pinpoint the proper position of a species among its relatives. These anomaly zones may create a little static in the signal, but the general message of phylogenetic trees can still be uncovered via careful large-scale analysis. In this case, the teams’ phylogeny showed that sexual parasitism evolved in the most recent common ancestor of modern anglerfish, likely aiding their adaptation to the deep-sea environment. This provides further support for the theory that this unique reproductive strategy not only addressed the challenges of mate scarcity but also played a role in the broader diversification of anglerfish species across extreme ocean habitats.Brownstein’s phylogenetic reconstruction of the anglerfish adaptive radiation serves as a telling example of environmentally-driven evolution, and the impact of this work extends far beyond the midnight zone. Both Brownstein and Near are particularly excited about the practical applications of their recent anglerfish research in relation to the human adaptive immune system. Near posits that if similarities exist between a human’s immune system and that of a fish, this could lead to great advances in research targeting organ transplantation, autoimmune disease, and other areas involving a misdirected adaptive immune function. The translational road from Ceratioidei to humans may not be a simple one, but Brownstein’s work has provided a valuable template for future endeavors into the deep, dark unknown.