A popular trope of science fiction is a world in which creatures with unusual body plans rule. From the octopoid Martians of War of the Worlds to the giant "bugs" of Starship Troopers, there is a creepy appeal in the idea that a race of spineless creatures could pose a real threat to humanity.
Because as far as we are concerned, the backbone is king. Whether or not we are truly the "dominant" organisms on Earth is debatable. But we are vertebrates – and so are most of the large, charismatic animals that walk, swim and fly. It is only natural that we find ourselves drawn to what Henry Gee, Senior Editor at Nature, calls "our own corner of creation".
The spine is certainly a useful innovation. It provides support for the body, as well as valuable protection for the spinal cord. The fact that our bodies are supported by an internal skeleton as opposed to an external one also allows for a greater range of movement, and means vertebrates can grow to far greater sizes than any invertebrate ever has.
But seeing as over 90% of all animals get by just fine without backbones, it is not obvious why this novelty arose in the first place. How did the spine emerge from a spineless world?
The evolutionary leap that birthed the vertebrates took place during the Cambrian period around 500 million years ago. Prior to this, life had been a pretty simple affair for hundreds of millions of years; single cells drifted around, occasionally getting together to form a colony. That was pretty much it.
We briefly possess notochords during our development in the womb
Then, boom! In an event known as the Cambrian explosion, Earth's oceans were filled with a huge array of life forms. Within a few tens of millions of years something new joined the ranks of the six-foot predatory arthropods and multi-eyed oddities. Animals that looked something like today's lampreys and hagfish.
These creatures were some of the first vertebrates. Their bodies were supported by rudimentary vertebrae and a stiff rod called a notochord made from a cartilage-like material. The notochord was the precursor to the backbone, the structure found in vertebrates from mice to dinosaurs to humans.
We know where these first vertebrates came from. Their predecessors are represented by fossils from those Cambrian seas: worm-like animals like Pikaia and Haikouella. These animals are not vertebrates, but they do possess a notochord. They belong in a more inclusive category called the chordates, which incorporates vertebrates and a few vertebrate-like groups.
It is worth noting that this means that we ourselves are chordates. In a throwback to our deep ancestry we briefly possess notochords during our development in the womb.
But the question of exactly where those first chordates came from has long proved controversial. In 1909, the golden jubilee of Darwin's On the Origin of Species, the Linnean Society of London organised an event to explore the origin of the vertebrates.
These early creatures were too squishy to leave much lasting evidence
It was not a rousing success: "The disputants agreed on one single point," quipped zoologist Thomas Stebbing: "namely, that their opponents were all in the wrong."
Over the years, virtually every invertebrate group – from molluscs to arthropods – has been suggested as a starting point for the origin of the chordates. The fossil evidence to reliably answer the question is lacking.
This is because unlike later vertebrates, which are full of hard, "fossilisable" components like bones and teeth, these early creatures were too squishy to leave much lasting evidence. Today, only faded imprints of their soft bodies remain.
The result is an early history documented by what palaeontologist Phillippe Janvier refers to as "squashed slugs". These are difficult to interpret, leaving plenty of room for speculation.
This means that we are, ultimately, defined by our anus
That said, in the past few decades the fields of evolutionary developmental ("evo-devo") biology and molecular phylogenetics have given scientists a much better understanding of the evolutionary relationships between organisms.
This has included the finding that some of our closest invertebrate relatives are a group of marine animals that includes the familiar starfish, sea urchins and sea cucumbers, as well as some unusual worm-like animals called the hemichordates. Like all of these animals, we are deuterostomes – meaning that during embryo development, our anus forms before our mouth.
In other words, we are vertebrates, which are a form of chordate, which are themselves a form of deuterostome.
This means that we are, ultimately, defined by our anus, which is a bit humbling. But this really is the best way scientists have come up with for organising the deepest divisions in the animal kingdom.
Though we appear to look nothing like sea urchins and their ilk, we do share a common ancestor, which according to Linda Holland, a chordate researcher at the Scripps Institution of Oceanography, USA, could have looked sea urchin-like, chordate-like, hemichordate-like - or like none of these.
Then, one of those early deuterostomes became the very first chordate by gaining a notochord.
The notochord is the supporting organ of the beating tail
Nori Satoh, a researcher at the Okinawa Institute of Science and Technology in Japan, has identified what he sees as the moment the notochord, and hence the chordate lineage, was born. "I have proposed that the occurrence of tadpole-like larvae is a key event that caused the evolution of chordates," he explains.
Early in life, many deuterostomes pass through a larval stage. But while acorn worm or sea urchin larvae might swim about by rhythmically moving tiny hair-like structures – cilia – on their bodies, chordate larvae have a tail that they beat.
"The notochord is the supporting organ of the beating tail," says Satoh.
Satoh's idea builds on the work of British zoologist Walter Garstang. In this hypothesis, the early chordates ended up forsaking an evolutionary future as bottom-dwelling invertebrates, and instead retained their larval notochords to adulthood – just as some species of amphibians retain larval characteristics into adulthood today.
In Satoh's lab, work is underway to demonstrate the genetic underpinnings that could result in such a transformation.
As for why it would be beneficial to evolve a larval tail in the first place, and then retain it into adulthood, Satoh thinks this is obvious. "Swimming with a beating tail is much more efficient than locomotion with ciliary beats," he says. "The notochord gave the earliest chordates a unique advantage."
Anyone who has experienced the discomfort of a "slipped disc" will appreciate how useful the notochord still is
In the dangerous Cambrian oceans, full of highly mobile predators, faster swimming would have been a valuable asset for a creature trying to outpace an attacker.
Over time, the chordate body plan gradually changed.
In most modern vertebrates – including humans - the notochord no longer provides support, but it still has an important role to play. It has become part of the discs that separate our vertebrae and that act as shock absorbers. Anyone who has experienced the discomfort of a "slipped disc" will appreciate how useful the notochord still is.
But structure and support in large vertebrates like humans is provided by the backbone itself.
"Presumably, as animals increased in size, it became advantageous to have something stronger than a notochord for the paraxial muscles to work against in swimming," remarks Holland.
A few living chordates still retain the ancient backbone-free condition where the notochord offers support. They can provide us with some intriguing glimpses into our evolutionary past.
The lancelet, or amphioxus, is a translucent, fish-like creature that represents one of the only surviving lineages of non-vertebrate chordates in the modern age. It is a "living fossil" that gives researchers like Holland an insight into how vertebrates evolved in those prehistoric oceans.
From our perspective, it is easy to see the later evolution of the vertebrates as a March of Progress
The anatomy of the lancelet hints at the spine's early evolution, as it possesses segmented muscles and a sheath around its notochord and nerve cord. The vertebral column in humans and other animals with a backbone is, put very simply, an elaboration of this same notochordal sheath.
Holland and her collaborators have shown that lancelets possess a basic set of genes that is also found in all modern vertebrates. However, we carry extra versions of this gene set, following two rounds of genome duplication in the early evolution of vertebrates. All those bonus genes could then take up new roles – like growing cartilage, or the special type of cells that ultimately help generate the bones in our skull and jaws.
A slightly later duplication event gave some early vertebrates another suite of genes that were eventually harnessed to mineralise softer tissues. They produced a more robust internal scaffolding: the vertebrate skeleton.
From our perspective, it is easy to see the later evolution of the vertebrates as a March of Progress: early vertebrates gave way to fish, which gained legs and became four-legged land animals, which eventually began walking on two legs and became human.
But viewing vertebrate history as a straightforward progression from humble origins to humanity is misleading.
When researchers at the European Molecular Biology Laboratory found a notochord-like structure in a marine worm back in 2014, it supported an old theory of how chordates originated from ancient worms.
Intriguingly, it also suggested just how wrong our march of progress image really is. The appearance of the notochord might not have been a seminal turning point in the history of life after all.
We might think that notochords are an evolutionary winning invention, but natural selection apparently thinks otherwise
In fact, the notochord might have appeared earlier, in our shared ancestor with starfish and other spineless deuterostomes. These creatures might then have given up on the structure, adapting to life on the seabed where a notochord was simply not a particularly useful feature.
Other animals might also have once had, and then lost a notochord. While lancelets are commonly identified as the closest living relatives of vertebrates, back in 2006 a paper in Nature claimed that this is not the case – pointing instead to tunicates, also known as sea squirts, as a better candidate.
Tunicates certainly are chordates, and have tadpole-like larvae to prove it, but their adult forms generally remain attached to rocks, and are essentially just filter-feeding blobs.
It seems that the tunicates, too, might once have had a chordate-like body plan, but then adapted to a simpler lifestyle in which carrying a notochord was unhelpful. We might think that notochords are an evolutionary winning invention, but natural selection apparently thinks otherwise.
Responding to these claims, long-time vertebrate enthusiast Gee highlighted what he described as our human-centric view of the progression of evolution. "History is written by the victors," he writes. "This is as true for our account of evolution as it is for purely human affairs."
A starfish is as highly-evolved as a human
"Rather than the steady acquisition of progressively more chordate-like (and, by implication, human-like) features from an ancestor with nothing much to recommend it, the story becomes one of persistent loss."
Sci-fi depictions of invertebrate supremacy may be a little off the mark, but numerically at least, our world is dominated by creatures that to us seem simple. Some even lack many of the traits we would associate with animals, such as mobility or a head.
Evolution has no end point. There is no ideal that it is striving towards. A starfish is as highly-evolved as a human, and the fact that an ancestral starfish may have shed some of the traits we associate with sophisticated body forms demonstrates the absence of innate vertebrate superiority.
So remember, there is nothing wrong with being spineless.
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