Arachnolingo 1: "True" spiders: are tarantulas "false spiders"?

 A few days ago, I was "corrected" on social media by a gentleman who explained to me that tarantulas and trapdoor spiders weren't actually spiders, but belonged in a different order of Arachnids.
While his unfailing confidence (a quality often found in people incorrectly correcting others) forced admiration, that gentleman was unfortunately very wrong.

Although not "true spiders", tarantulas truly are spiders

In fairness to him, though, he was not the first, nor the only one to make that mistake. Common names are often a source of confusion, and there's no finer example of that than "true spiders", the English common name of the infraorder Araneomorphae.
It seems to imply that tarantulas, trapdoor spiders and the like, which aren't part of that group, are some sort of "false spiders" that are similar and related, but not bona fide spiders.
Let's talk basic spider taxonomy.

Spiders, along with scorpions, harvestmen, "camel spiders" (Solifugae), mites and ticks, vinegaroons, and other, less famous groups, are one of the orders of the class Arachnida, the Arachnids. The relationships between the different orders of Arachnids, as well as the exact limits and composition of the group, are still not completely resolved. Depending on the different studies, 11 to 13 orders are included in the class Arachnida, and spiders are one of them.

The class Arachnida and some of its representatives

Spiders (order Araneae), on the other hand, are quite clearly defined. All spiders share a number of unique trademark features ("synapomorphies" for those who speak scientist), such as the presence of spinnerets on the abdomen, which produce silk, palps transformed into copulatory structures (involved in mating) in males, and chelicerae with two segments, the second one modified into a sharp, needle-like fang, associated with venom glands (although one spider family seems to have lost its ability to use venom).

External anatomy of a spider (from Dippenaar-Schoeman & Jocqué, 2008)

Extant representatives of the order Araneae are divided into two suborders: Mesothelae and Opisthothelae.
Mesothelae (whose name means "spinnerets in the middle") are very strange and ancient spiders, which are, nowadays, only represented by two families, Heptathelidae and Liphistiidae. Both are only found in Asia. They are very unusual spiders that retain visible segments on the abdomen, with a series of hard dorsal plates. They also have more than 6 spinnerets (8 or 6 + one pair fused into one) which are placed under the abdomen, right behind the lungs, far from the anal tubercule. Because of their dorsal plates, they're sometimes called "armoured trapdoor spiders" or "segmented trapdoor spiders". There are only 174 known modern species of Mesothelae.

The vast majority of modern spiders (more than 50 000 described species) belong in the other suborder, Opisthothelae. Their name means "spinnerets at the rear", as, unlike Mesothelae, their spinnerets sit at the posterior tip of the abdomen, right beneath the anal tubercule, widely separated from the pulmonary and genital openings. They differ from Mesothelae in their complete absence of visible abdomen segmentation. They also have fewer spinnerets than Mesothelae, never more than 6 (the fourth pair is lost or modified).
Unless you're in East or Southeast Asia and know exactly what you're looking for (or get incredibly lucky), any spider you've ever seen and will ever see belongs to the suborder Opisthothelae.
 

The underside of a typical Opisthothelae (a young Segestria florentina) showing the wide space separating the spinnerets (red arrow) from the genital opening (yellow arrow, not fully formed as it is a juvenile specimen) and booklungs (green arrow). The blue arrow points to the anal tubercule.

 

The suborder Opisthothelae is further subdivided into two infraorders: Mygalomorphae, which includes tarantulas, trapdoor spiders and the like, and Araneomorphae, the "true spiders".

The order Araneae (spiders) is divided into two suborders, Mesothelae and Opisthothelae; the latter is itself divided into two infraorders, Mygalomorphae and Araneomorphae.

Araneomorphae is, by far, the most speciose of all subgroups of spiders: there are currently over 47 000 described species, found all over the world.
The spiders you're most familiar with, either because you've seen them in person or heard about them, belong in that infraorder: jumping spiders (family Salticidae), orb weavers (Araneidae and Tetragnathidae), huntsman spiders (Sparassidae), wolf spiders (Lycosidae), cobweb and widow spiders (Theridiidae), violin or "recluse" spiders (Sicariidae), and many others (97 families!), are Araneomorphae.

Araneomorphae ("true" spiders) are an incredibly diverse group, which includes the vast majority of extant spider species

They are incredibly diverse and varied, and come in all shapes and sizes, from the size of a pinhead to a legspan approaching the diameter of a dinner plate. They often have eight eyes, sometimes six, rarely four, two or zero. Most of the time, "true spiders" have two booklungs, but a few families have a second pair. A lot of them hunt with these beautiful webs we're all familiar with, but most of them actually don't (all spiders can produce silk and make some use of it, though).
However, despite their diversity, Araneomorphae all share two unique features that aren't found in other spider groups; while one isn't exactly easy to observe, the other one is visible at first glance.
Like the Mesothelae, Araneomorphae start off with four pairs of spinnerets; however, while they develop in the egg, one of the pairs turns into a modified silk-producing organ, the cribellum, or becomes reduced into a vestigial organ, the colulus.
Fortunately, the second trademark feature of Araneae is much easier to spot: unlike Mesothelae and Mygalomorphae, their chelicerae face each other, fangs turned inwards, and move in a clamp-like motion. This orientation is called labidognath or diaxial.

This wolf spider's (Lycosa tarantula) wide open chelicerae are labidognath: they face each other, which is indicative of an Araneomorph (a "true spider").

 

The other infraorder of Opisthothelae, Mygalomorphae, doesn't really have a common name in English. That's not exactly surprising, as most Mygalomorphae are very secretive and seldom seen.
Tarantulas (family Theraphosidae) are by far the most famous (and the only Mygalomorphs the layperson is vaguely familiar with), and also the most diverse: this single family contains almost a third (more than 1000 species) of all described Mygalomorph species. Other somewhat notorious members of this infraorder include Australian funnel-web spiders (family Atracidae), purse-web spiders (Atypidae) and a number of families known as trapdoor spiders.
In total, Mygalomorphae includes 33 families and about 3500 species, but they're still poorly known and their true diversity is underestimated. 

While they tend to be, on average, larger than Araneomorphae, they come in any size, from tiny to huge: the smallest species are about 1 mm long as adults, while the largest can reach up to 10 cm in body length and 30 cm in legspan.
Like Araneomorphae, they're found all over the planet, but most of them are rarely seen due to their mainly subterranean, and highly sedentary lifestyle. Except for mature males looking for mates, it's not common to see them strolling around, particularly during daytime. Although some make webs (often connected to an underground retreat) and a few are free-living, most Mygalomorphs live in burrows, whose entrances are often equipped with elaborate trapdoors, turrets or other structures made of silk and debris.

Many Mygalomorphs, like purse-web spiders (Atypidae), are secretive, seldom-seen oddballs with a mainly subterranean lifestyle

Mygalomorphae all share a number of traits that make them fairly easy to recognise. The most prominent of these features is probably their chelicerae, which, unlike those of Araneomorphae, are parallel and projected in front of the body, and move mainly in a vertical motion, with the fangs folding under the basal segments of the chelicerae, kinda like a pocket knife. This cheliceral orientation is called "orthognath" or "paraxial". Although there are exceptions (Actinopodidae, the southern mouse spiders, have a very wide eye field), their eight eyes are most often grouped in a small, dense cluster.
They also have two pairs of booklungs, while most Araneomorphae have only one.
Finally, their pedipalps tend to be fairly long, much longer on average than those of Araneomorphae, sometimes giving the false impression that they have ten legs.

This very defensive Harpactira tigrina almost flipped on its back, displaying its orthognath chelicerae, four pairs of booklungs (red arrows) and long pedipalps: the marks of a typical Mygalomorph

However, none of these features is unique to Mygalomorphae: orthognath chelicerae and long, leg-like pedipalps are also found in Mesothelae; tightly clustered eyes are found in Mesothelae and some Araneomorphae, as well as the two pairs of booklungs.
There is, nonetheless, one unique trait that is shared by all mygalomorphs: they all have a maximum of six spinnerets, most often less than that (four, some only have two), and, unlike in Araneomorphae, there's no trace of the fourth pair, not even during development.
In practice, you don't need a close look at the spinnerets to recognise them, though: any spider with orthognath chelicerae but no visible segmentation on the abdomen is a Mygalomorph.

While they are not part of the group known as "true spiders", Mygalomorphae, including tarantulas, have spinnerets which produce silk, chelicerae with fangs that can inject venom, and males have modified pedipalps they use for mating; so do Mesothelae (although they were believed to be venomless for a long time). That makes them spiders. Real, full, bona fide spiders.
They may not be "true spiders", but they are true spiders; there is no ambiguity in that fact, except the confusion caused by a misleading common name.⏹

Numbers of spider species and families change very quickly: new species are discovered every day, and new studies often change the classification and delimitation of the families. This article was last updated on Dec. 14, 2022, and provides numbers as they were at this date.

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Except when the source is explicitly cited, the images illustrating this blog are mine and are not free to use.