Increasing morphological complexity in multiple parallel lineages of the Crustacea

Abstract

The prospect of finding macroevolutionary trends and rules in the history of life is tremendously appealing, but very few pervasive trends have been found. Here, we demonstrate a parallel increase in the morphological complexity of most of the deep lineages within a major clade. We focus on the Crustacea, measuring the morphological differentiation of limbs. First, we show a clear trend of increasing complexity among 66 free-living, ordinal-level taxa from the Phanerozoic fossil record. We next demonstrate that this trend is pervasive, occurring in 10 or 11 of 12 matched-pair comparisons (across five morphological diversity indices) between extinct Paleozoic and related Recent taxa. This clearly differentiates the pattern from the effects of lineage sorting. Furthermore, newly appearing taxa tend to have had more types of limbs and a higher degree of limb differentiation than the contemporaneous average, whereas those going extinct showed higher-thanaverage limb redundancy. Patterns of contemporary species diversity partially reflect the paleontological trend. These results provide a rare demonstration of a large-scale and probably driven trend occurring across multiple independent lineages and influencing both the form and number of species through deep time and in the present day.Arthropoda ͉ correlates of diversity ͉ disparity ͉ macroevolutionary trend ͉ tagmosis M ost of the natural sciences operate by documenting patterns and trends and thereby formulating general rules. Evolution, however, is an essentially contingent process, meaning that evolutionary trajectories can rarely be predicted. Proposed evolutionary trends, such as Cope's rule for evolutionary size increase within lineages, have generally turned out to be only weakly predictive, either resulting from passive diffusion away from some barrier (1-4) or applying only at local temporal and taxonomic scales (5-9). Here, we demonstrate a remarkable and pervasive trend for increasing morphological complexity in multiple parallel lineages of the Crustacea [the major arthropod group with the longest and most disparate fossil record (10)] throughout the Phanerozoic. Previous studies by Cisne (11) and Wills et al. (10) have shown that average complexity, as indexed by the serial differentiation and specialization of limbs along the body axis (a process known as tagmatization or tagmosis), increased from the Cambrian to the present. However, this pattern could have resulted from nothing more than random diffusion from a minimum boundary (1,12,13) or from the differing fortunes of a small number of clades that happen coincidentally to differ in complexity, rather than from a pervasive and driven trend within most clades (see Fig. 1). This work uses recently available phylogenetic evidence that allows us to distinguish between these (and other) possibilities.To understand the mechanisms by which the average complexity of crustaceans increased throughout the Phanerozoic, this article addresses a range of related questions. Did many parallel lineages evolve fr...

Evolution of functional specialization and division of labor

“…For example, in many arthropods iterated body segments carry appendages that are involved in multiple functions such as foraging and locomotion (13,37) or walking and burst swimming (38). Another example fitting within our framework, and one that we explore in some depth later, is pairs of duplicated genes coding for bifunctional gene products.…”

“…In addition to physical castes, ants (and many social bees and wasps) go through ontogenetic stages in which individuals fulfill different tasks, but the total number of temporal and physical castes rarely seems to exceed six (15). Similarly, it has been noted that polymorphisms are conspicuously absent from some taxa of colonial marine invertebrates (23) and that limb differentiation in crustaceans consistently increased over geological time but never reached the highest possible complexity indexes (37). It is furthermore clear that many genes and cells fulfill a multitude of tasks.…”

Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation

“…This connection between speciation and morphological evolution is partly consistent with traditional formulations of punctuated equilibrium 7 , whereby the speciation process itself leads to morphological change. However, an alternative explanation for this result is that phenotypic evolvability-the capacity of lineages to evolve morphological and ecological novelty-itself promotes speciation 40,41 . Many biologists already recognize this notion intuitively as the mechanism by which ecological key innovations promote diversification during adaptive radiation [42][43][44] .…”

Clades reach highest morphological disparity early in their evolution

“…The prevalence of early high disparity as the dominant pattern of clade evolution ranks alongside the well-known tendencies for increasing complexity (7,8,71,72) and diversity (2, 8) underpinning putative macroevolutionary trends of the widest possible generality. Moreover, it seems to apply throughout the Phanerozoic, and not merely at times of global diversification (e.g., the early Paleozoic).…”

“…Nonetheless, the prospect of formulating and testing macroevolutionary generalities is extremely seductive, because they seem to offer fundamental insights into the manner in which evolutionary processes operate throughout Earth's history (2). Patterns of increasing diversity (measured via proxies of species richness) (3,4) and increasing maximal organismal size within clades (Cope's rule) (5) have been perennial foci, whereas more recent attention has turned to supposed trends in increasing organismal complexity (6,7) and the mechanisms that might generate them (8). This paper tests another putative generality, namely, the tendency for taxa to reach maximal morphological diversity (disparity) relatively early in the lifespan of their parent clade (9-17) (early high disparity).…”