Ceratioidei

Ceratioidei, the deep-sea anglerfishes or pelagic anglerfishes, is a suborder of marine ray-finned fishes, one of five suborders in the order Lophiiformes, the anglerfishes. These fishes are found in tropical and temperate seas throughout the world, living above the bottom of the deep sea, in the pelagic zone.

The deep-sea anglerfishes exhibit extreme sexual dimorphism; the males are many times smaller than the females. To reproduce, a male seeks out a female, using his sharp teeth-like denticles to clamp onto the female. The details of this sexual parasitism varies between the species; in a number of species the male permanently becomes part of the female, their tissues fusing with each other. This is the only known natural example of a process called parabiosis. The esca, the defining feature of all anglerfish groups, are bioluminescent in the deep-sea anglerfishes, attracting prey in the vast darkness of the bathypelagic zone which they inhabit.

Ceratioidei takes its name from the genus Ceratias, the type genus of the family Ceratiidae and of the suborder. Ceratias means "horn bearer", an allusion to the esca sticking up from the snout being likened to a horn.

Ceratioidei was first proposed as a grouping in 1912 by the English ichthyologist Charles Tate Regan as the division Ceratiformes within the suborder Lophoidea of the order Pediculati, which included the Batrachoididae. The Batrachoididae are no longer considered to be closely related to the anglerfishes, which are now included in the order Lophiiformes; within that clade the Ceratioidei are in the same clade as the Chaunacoidei with the Antennarioidei and the Ogcocephaloidei as the sisters of that clade. The 5th edition of Fishes of the World treats this grouping as a suborder within the Lophiiformes.

Classification of this suborder is largely based on characters specific to the females, such as the escal morphology, though some osteological characteristics and meristics are shared between the sexes. Male anglerfish can be identified to the genus level using characteristics of the denticular "teeth" and nostril morphology, but species-level identification has not been possible, even when examining parasitic males.

Ceratioidei contains the following families:

It is presumed that Ceratioids derive from an ancestor resembling modern Chaunacoids (deep-sea sea toads) or Ogcocephaloids (batfish), which lived in benthic or littoral habitats, which eventually retained the pelagic habits of the Lophiiform larva into adolescence. Monophyly is supported in this group through the shared characters of extreme sexual dimorphism, loss of the ambulatory pelvic fins found in other anglers, relocation of the pectoral fins, and a general reduction in density through the loss of bony parts, decrease in ossification and muscle mass, and the infusion of lipids throughout the body.

Sea toads (such as Chaunacops, top) and batfish (Ogcocephalus, bottom) may resemble the ancestors of deep-sea anglerfish before they became pelagic

A 2024 study found that while the Ceratioids likely diverged from the Chaunacidae during the Paleocene, the diversification into their various extant families only occurred throughout the Eocene, following the Paleocene-Eocene Thermal Maximum. This likely also coincides with their colonization of deep sea habitats. Prior to these radiations, ancestral Ceratioids evolved extreme sexual size dimorphism and independently lost adaptive immune genes such as aicda, which allowed male anglerfishes to fuse with females, ultimately leading to the evolution of their sexual parasitism.

One explanation for the evolution of sexual parasitism is that the relative low density of females in deep-sea environments leaves little opportunity for mate choice among anglerfish. Females remained relatively large to improve fecundity: a larger female would be able to have volumetrically larger ovaries and eggs. Males would be expected to shrink to reduce metabolic costs in resource-poor environments and would develop highly specialized female-finding abilities. If a male is able to find mates and permanently associate with them (eventually leading to the development of fusion), then it is ultimately more likely to improve lifetime fitness relative to free living males, particularly when the prospect of finding future mates is poor; as an attached male is always available to the female for mating, he can potentially participate in multiple fertilization events, ensuring paternity for every such event where he is attached. Comversely, higher probabilities of male-female encounters within a habitat might correlate with species that demonstrate facultative parasitism or a more traditional temporary contact mating.

Owing to the extreme environments they inhabit, fossil remains of deep-sea anglerfishes are very rare in the geologic record. Only a few formations worldwide preserve them, which tend to have been deposited in tectonically active regions where deep-sea sediments could be uplifted to the surface. These include the Puente Formation of California, USA, and the Kurasi Formation of Sakhalin Island, Russia. These formations date to the mid-late Miocene, and specimens recovered from them are assigned to extant genera.

Sexual parasitism is a mode of sexual reproduction unique to the Ceratioidei facilitated by their extreme sexual dimorphism. The core of the behavior is the physical attachment of the males onto the female's body for reproduction, which is further separated into three categories: obligatory parasitism, where the males need to permanently attach to the females and fuse their tissues together; temporary nonparasitic attachment, in which males are able to live independently; and facultative parasitism, where both parasitic attachment and independent males occur. The term "sexual parasitism" is used because the males in the obligate-parasitic species are incapable of feeding after metamorphosis, and must latch onto the female to acquire nutrition, akin to an ectoparasite. If they don't find a mate, the males are presumed to die. Furthermore, sexual maturation in these species is triggered by the attachment of the male to the female. This behavior has evolved multiple times within the group, having developed independently 3 to 5 times; the diversity in the nature and location of the males' attachment being evidence of independent evolution.

Generally, the males locate their mates through a combination of visual and olfactory means, though some species are thought to specialize in one sense at the cost of the other: with some relying solely on vision, possessing an unusually wide binocular field of vision to detect bioluminescent caruncles on the dorsum of females (Ceratiidae), or exceptionally developed olfactory structures within their nostrils to detect female pheromones (Gigantactinidae). In some families, such as Centrophrynids and Neoceratiids, the methods males use to locate females remain unclear.

In obligate parasitic species, the male bites into the female's skin using the "denticular apparatus", beginning the process of fusion and eventually receiving nutrients via their connected circulatory systems, though he retains functional gills and provides for his own oxygen needs; the male's attachment point, an outgrowth of the female's tissue resembling a nipple or a stalk, often leaves a gap where water can flow through his mouth and out the gills. In the toothed seadevil, where the males were observed to attach so completely that they often lacked any remaining oral opening, respiration is thought to occur through pumping water in and out of the opercular openings, as the gills remain well-developed. After fusion, males increase in volume and often become much larger relative to free-living males of the species, and the longer a male is attached, the more atrophied his body becomes. Though sensory organs like the eyes and nostrils degenerate, the hearts, gills, and fin rays of males are retained.

This parasitism has developed to the point that, at least in Ceratiids and some leftvents, both sexes never mature (their gonads do not ripen) before fusion takes place. After fusion, they live and remain reproductively functional as long as the female stays alive, and can take part in multiple spawning events; this union of the female and male has been referred to as a single hermaphroditic organism. Multiple males can be incorporated into a single individual female, with up to eight males attaching almost anywhere on the body in the triplewart seadevil, though some taxa appear to have a strict one male per female rule, such as Linophryne spp., where males almost always attach to the ventral midline, in front of the female's genital opening. This method ensures that when the female is ready to spawn, she has a mate immediately available, which was surmised by Charles Tate Regan;

Subsequent studies discovered that the sexes of even the smallest larvae (2-3 mm in total length) can be determined through the early development of the illicium, appearing as a small undifferentiated papilla on the snout of female larvae; thus the idea of sex being determined through attachment and non-attachment is unfounded.

In non-parasitic species, so far including black seadevils, footballfishes, double anglers, whipnose angler, and most genera of dreamers; both sexes mature independently, without requiring fusion, with the males attaching temporarily. Indeed, there is no evidence of sexual parasitism, and where males of the black seadevils were observed to attach firmly to their mates, there was no evidence of fusion. The denticular apparatus in these males enable them to attach to the females and presumably to capture prey items as well, as food has been found in some males of these species, and they continue to grow after metamorphosis even after depleting the energy stores within their livers. It is probable that these males only attach to females once they are ready to spawn.

Facultative parasitism is known in fanfins and the plainchin dreamarms and Bertella, the latter pair being Oneirodids. This method is an intermediate between non-parasitism and obligate; both sexes mature independently, but males attach regardless of the female's maturity. If both are sexually mature, they spawn, fertilization occurs, and the male presumably detaches to recover, feed, and search for another mate. If either partner aren't ready to spawn, the male attaches until they are ready; the longer he remains attached, the greater the chances are of him fusing and becoming a sexual parasite.

The effective loss of certain aspects of ceratioid immune systems, such as the adaptive immune system, is a key factor in allowing the fusion between the sexes. It is assumed they have evolved new immune strategies which compensate for the loss of B and T lymphocyte functions found in animals with an adaptive immune system.

The phylogenetic tree below is based on Pietsch & Orr (2007);