Parallel evolution controlled by adaptation and covariation in ammonoid cephalopods

Abstract

BackgroundA major goal in evolutionary biology is to understand the processes that shape the evolutionary trajectory of clades. The repeated and similar large-scale morphological evolutionary trends of distinct lineages suggest that adaptation by means of natural selection (functional constraints) is the major cause of parallel evolution, a very common phenomenon in extinct and extant lineages. However, parallel evolution can result from other processes, which are usually ignored or difficult to identify, such as developmental constraints. Hence, understanding the underlying processes of parallel evolution still requires further research.ResultsHerein, we present a possible case of parallel evolution between two ammonoid lineages (Auguritidae and Pinacitidae) of Early-Middle Devonian age (405-395 Ma), which are extinct cephalopods with an external, chambered shell. In time and through phylogenetic order of appearance, both lineages display a morphological shift toward more involute coiling (i.e. more tightly coiled whorls), larger adult body size, more complex suture line (the folded walls separating the gas-filled buoyancy-chambers), and the development of an umbilical lid (a very peculiar extension of the lateral shell wall covering the umbilicus) in the most derived taxa. Increased involution toward shells with closed umbilicus has been demonstrated to reflect improved hydrodynamic properties of the shell and thus likely results from similar natural selection pressures. The peculiar umbilical lid might have also added to the improvement of the hydrodynamic properties of the shell. Finally, increasing complexity of suture lines likely results from covariation induced by trends of increasing adult size and whorl overlap given the morphogenetic properties of the suture.ConclusionsThe morphological evolution of these two Devonian ammonoid lineages follows a near parallel evolutionary path for some important shell characters during several million years and through their phylogeny. Evolution of some traits (involution, umbilical lid) appears to be mainly driven by adaptation to improve the hydrodynamic properties of the shell, whereas other characters (sutural complexity) evolved due to covariation with features that play a central role in the morphogenesis of mollusc shells. This example provides evidence that parallel evolution can be driven simultaneously by different factors such as covariation (constructional constraints) and adaptation (natural selection).

Globacrochordicerasgen. nov. (Acrochordiceratidae, late Early Triassic) and its significance for stress-induced evolutionary jumps in ammonoid lineages (cephalopods)

“…an increase of shell involution), and (3) the clade furthermore experienced an increase of indentation of its suture line. Multiple ex- amples of similar morphological trends in ammonoid shells have already been illustrated and discussed (e.g., Haas 1942;Guex 1973Guex , 1992Guex , 2006Thierry 1982;Bayer & McGhee 1984;Kennedy & Wright 1985;Dommergues et al 1989;Dommergues 1990;Klug et al 2005;Monnet et al 2011Monnet et al , 2012De Baets et al 2012). The increasing body size of the studied lineage conforms with Cope's rule, known as the widespread tendency of animal groups to evolve toward larger body size (Newell 1949;Rensch 1960;Gould 1966).…”

“…As discussed by Monnet et al (2011), such trends in ammonoid shell (which acts as a buoyancy apparatus) could reflect that their morphology is mainly controlled by adaptive and constructional constraints.…”

“…The classical morphofunctional interpretation (often called the Buckland hypothesis) is that increasing suture indentation leads to forms adapted to deeper water depth, because it is supposed to provide buttressing against hydrostatic pressure on the phragmocone (Buckland 1836;Pfaff 1911;Saunders 1995;De Blasio 2008;and references inside). However, this function of the septal folding remains controversial (Saunders 1995;OlÕriz et al 2002;Lewy 2002) and constructional constraints complicate its interpretation (see discussion in Monnet et al 2011) leading to the idea that the evolution of the suture indentation of ammonoids exceeds their functional needs or limits.…”

“…Size increase is commonly interpreted in terms of adaptive advantages such as increased defence against predation, increased food competition, increased success in mating, increased individual longevity and/or better energy use, among others (Stanley 1973;Brown & Maurer 1986;Hone & Benton 2005). For ammonoids, several authors illustrated and discussed examples of increasing ammonoid shell size (Stanley 1973;Hallam 1975;Thierry 1982;Guex 2003;Dommergues et al 2002;Monnet et al 2011Monnet et al , 2012De Baets et al 2012).…”

“…Furthermore, the possible influence of facies changes recorded at the Spathian/Anisian boundary (see below) is also reduced. Indeed, several authors discussed the possible relationships between ammonoid shell shape and facies (Jacobs et al 1994;OlÕriz et al 1997;Kawabe 2003;Wilmsen & Mosavinia 2011; further references in Monnet et al 2011) but without a clear consensus. In the northern Humboldt Range, the depositional environment of strata of haugi Zone age does not significantly differ from that of the younger Anisian faunas (i.e.…”