Most animal clades follow a predictable path in geographic commonness and taxonomic diversity over time1,2. Clades usually start within a very restricted range3, and then expand and diversify to occupy large stretches of Earth. Almost immediately after this peak in success, they start declining in diversity and finally go extinct1,2,4,5,6 (although a few may survive with as little diversity as one genus like sphenodonts, coelacanths, and nautiloids). There is no consensus about the reasons underlying this path, and no general explanation has been advanced as to why clades have to die out following such a predictable path7. Studies of paleontological extinctions deal with the ever-increasing negative effect of biotic interactions8, geologic and climatic events1,2, ecological and evolutionary traps9, and of course major extinction crises10. While these factors certainly represent effective causes for extinction of species, their impact at the level of clades is unclear, although it has been demonstrated that competition may drive entire clades extinct11,12. With the exception of clades that fail during mass extinctions, we argue the explanation for the demise of most other clades lies in the tendency of natural selection to produce more and more specialised types within each lineage as time progresses13,14, a pattern we dubbed weak directionality (in contrast to old views of evolution as moved towards the “perfection of life”)13. Herein we define specialisation as a process of adaptation to a specific habitat via the acquisition of narrow ecological niches15, and infer the degree of specialization by the dynamics of species range size and its mutual overlap among species within clades. While specialization confers obvious advantages in terms of competitive abilities where and when species do live16, it also increases extinction risk17,18,19,20,21, via reduction in range size9,10,22, and by depressing cladogenesis23,24. According to this “weak directionality” model13, clade geographic range and taxonomic diversification is best viewed as proceeding according to two distinct phases (Fig.1): during the early phase species richness increases, and the clade expands geographically. The intensity of competition and the extinction rate are low on average. But as the clade diversifies its total occupied range fills the available ecological space, thus depressing geographical expansion and greatly strengthening the effects of competition7,8,24,25. During this stage, specialisation might further foster taxonomic diversity, by promoting species coexistence, hence sympatry26,27,28. Yet, it also drives the clade into a late phase when its negative effects of survival and diversification will eventually take their toll on clade survival.

Figure 1: The weak directionality theory of clade geographic evolution. (A) The total (green solid line), average (blue solid line), and clade (gold solid line) range size curves for the focal clade. The total range curve is computed as the algebraic sum of individual species range sizes over time. The average range curve is computed dividing the total curve for the number of species present in each time bin. The clade range curve represents the range actually occupied by the entire clade, summed over consecutive time bins. According to weak directionality theory predictions, after the shift point (vertical light blue line) the total- and the clade range curves should diverge signficantly over time, as an effect of a progressive increased range overlap (sympatry). The area test (B) is devised to test such prediction. As species range sizes are expected to decrease, on average, after the shift points, the average range curve should take a negative slope after the shift (C). The slope test is devised to test such prediction. Full size image

The most direct expectation of weak directionality is that clades should become rich in specialised species as time passes. Hence, under this theory, we predict that most species in the late phase of clade evolution should have traits typical of specialists, such as small range size and high degree of sympatry17,18,29,30. Given high degree of sympatry and reduced range size are presumed to depress diversification, according to this model there should be some point in time where both the regime of range size evolution and the diversification process shift (Fig. 1). We tested this hypothesis by locating statistically significant shift points in the total range size, degree of sympatry, and net diversification rate curves. We then tested four hypotheses consistent with the early/late phases scenario to assess whether 1) our data support the existence and temporal coincidence of total range size, degree of sympatry, and diversification shifts, 2) the degree of sympatry increases and the net diversification rate decreases after the shifts, and 3) the average species range size decreases after the shifts (see Fig. 1) and 4) the degree of sympatry is negatively correlated to speciation rate and positively correlated to extinction rate, which would indicate the link between specialisation and the decrease in diversification.

To test these predictions we collected from the Paleobiology Database (https://paleobiodb.org/#/ on 2/10/2016) the fossil occurrence data on 21 extinct animal clades belonging to five different phyla (Cnidaria, Mollusca, Brachiopoda, Arthropoda, and Bryozoa, see supplementary information). The data included 14,430 species and 84,454 fossil occurrences, spanning around 480 million years from the early Cambrian trilobites and brachiopods, to late Cretaceous ammonites.

For all of the analysed clades, we first computed the range size of each species per time bin, and the range size of the entire clade per time bin, which represents the union of individual species ranges (Fig. 2). We then summed individual species ranges within each time bin and then over consecutive time bins, to produce a “total range curve”. The use of cumulative range values, rather than time bin data, is appropriate as it smooth off unequal sampling and allows calculating effectively changes in the regime of geographical evolution of clade (see below). The (slope of) total range curve plotted versus time indicates the velocity of range size accumulation at the level of clade. It is equivalent to the average size of species ranges times species richness cumulated over all time bins. The total range curve is best fitted by either sigmoid, or generalized logistic curves, while the linear model is rejected for all the examined clades. This indicates that the increase in total range size slows down towards the recent, according to saturation dynamic (Table 1). To quantify the degree of sympatry (Figs 1B and 2), we started by summing the geographic range of the entire clade over consecutive time bins. This “clade range curve” is different from the total range curve in that it depends on how much individual species ranges do overlap (for instance, if two species have range = 1 km2 and do perfectly overlap the total range curve will be 1 + 1 = 2 km2, while the clade range curve will be 1 km2, Fig. 2). Then, we computed the area between total and clade range curves per unit time, under the specific hypothesis that the area difference between the two curves should be larger after the shift point, thereby indicating a higher degree of sympatry since (Fig. 1B). Eventually, we tested how often the difference between the two curves tends to increase after the shift points across clades, in keeping with our hypothesis 2, by means of the binomial distribution.

Figure 2: Difference between total and clade range curves computation. The total geographic range is computed by summing the range of each species in each time interval and then over successive intervals. The actual range is the real range of the clade, thus it is computed as the union of species’ areas, subsequently summed over consecutive time bins. In the figure, the shaded areas represent the species ranges. Species are indicated by capital letters. For each time bin, extinct species are indicated in grey color, living species are reported in black. Upper row: computation of the total range curve. Lower row: computation of the clade range curve. Full size image

Table 1 Likelihoods obtained by comparing total range size cumulative curves to three different theoretical curves corresponding to the linear, sigmoid, and generalized logistic models. Full size table

The net diversification rate was computed starting from the fossil record as the expected number of speciation/extinction events per lineage per Myr. Finally, we computed a second measure of the degree of sympatry at the level of bin. For each such bin, we took the ratio between the total range size (summed algebraically over all species in the bin) and the clade range size in the focal interval. This ratio represents the degree of overlap among individual species ranges. We assessed whether changes in the degree of sympatry throughout a clade’s history significantly correlates with temporal variation in speciation and extinction rates. To this aim, we fitted birth-death models in which speciation and extinction rates respond to changes in sympatry by means of an exponential correlation with parameters γ λ and γ μ , respectively11.

Shift points in degree of sympatry among species, total range size and net diversification rate are statistically closer in time to each other than expected by chance in 20 out of 30 cases, and for 16 out of 21 clades (Table 2). Both figures are statistically different from chance according to the binomial distribution (Table 3), indicating that the existence and temporal coincidence of shift points are robust. We then took the average ages of the three shifts to get a single shift point, and tested hypotheses 2 and 3. In keeping with our predictions (hypothesis 2) the degree of sympatry increases after 28 out of 30 shift points. Even after excluding the earliest third of clade evolution (when a high degree of sympatry is expected because in a diversifying clade species tend to place close to each other on Earth’s surface5) we recover the same pattern. The increase is temporally coincident with shift points (Table 3).

Table 2 Average age of the shiftpoints (in Ma) and the percentage of time since clade inception to the shiftpoints. Full size table

Table 3 The distribution of positive cases (i.e. either in accordance or not with the hypotheses tested) for the clade statistics reported in Table 2. Full size table

Then, we tested the prediction that species average range size decreases after the shift points (hypothesis 3), by dividing the total cumulative range curve by the number of species present in each time bin. This allows testing the evolution of species average range size over time (Fig. 1A,C). After the shift points this curve has a slope significantly different from zero fifteen times, 12 of them being negative (i.e. the species average range size decreases towards the recent, Table 3), and in eight different clades. This is consistent with the idea that species after the shifts tend to be small-ranged and therefore specialists. Yet, after nearly one half of the averaged shifts (16/31, 51.6%) there was no significant pattern in average range size.

Net diversification rates decrease after the shift points in 28 out of 30 cases and for all of the clades, thus supporting our predictions.

Finally, as expected the extinction rates are positively correlated with the degree of sympatry in 12 clades out of 21, and the speciation rate is negatively correlated to sympatry in 13 clades (Table 4). Overall, 16 clades out of 21 show either decreased speciation or increased extinction as the degree of sympatry increases, in keeping with our prediction that sympatry (as a consequence of specialisation) depresses diversification to drive the clade extinct.

Table 4 Correlation between the degree of sympatry and speciation and extinction rates. Full size table

Overall, our results indicate that the distinction between an early and a late phase of clade evolution is useful, that the net diversification rate decreases consistently during the late phase, and that mainly specialist species, having high degree of range overlap to each other (sympatry), make up the majority of clade biodiversity after the shift points.

We repeated all of the analyses excluding species with less than 10 total occurrences, in order to rule out the possibility that what we perceive as rarity, is in fact lack of preservation. The results are available as supplementary information. On such a reduced dataset, we located 22 shift points for seventeen clades. The shift points are statistically significant in 19 out of 22 cases (86.4%), and net diversification rate is always lower after than before the shifts. Yet, the degree of sympatry after the shift is higher than before only 9 times, and the average range size is significant and negative just one time. Taken at face value, these latter results are not supportive of weak directionality. Yet, it must be noted that by excluding rare (or otherwise poorly sampled) species from the dataset, we effectively removed those species whose effect on clade range size evolution we were seeking to test.