Habitat and developmental constraints drove 330 million years of horseshoe crab evolution

Abstract

Records of evolutionary stasis over time are central to uncovering large-scale evolutionary modes, whether by long-term gradual change or via enduring stability punctuated by rapid shifts. The key to this discussion is to identify and examine groups with long fossil records that, ideally, extend to the present day. One group often regarded as the quintessential example of stasis is Xiphosurida, the horseshoe crabs. However, when, how and, particularly, why stasis arose in xiphosurids remain fundamental, but complex, questions. Here, we explore the protracted history of fossil and living xiphosurids and demonstrate two levels of evolutionary stability: developmental stasis since at least the Pennsylvanian and shape stasis since the Late Jurassic. Furthermore, shape and diversity are punctuated by two high-disparity episodes during the Carboniferous and Triassic – transitions that coincide with forays into habitation of marginal environments. In an exception to these general patterns, body size increased gradually over this period and, thus, cannot be described under the same, often-touted, static models of evolution. Therefore, we demonstrate that evolutionary stasis can be modular and fixed within the same group at different periods and in different biological traits, while other traits experience altogether different evolutionary modes. This mosaic in the tempo and mode of evolution is not unique to Xiphosurida but likely reflects variable mechanisms acting on biological traits, for example transitions in life modes, niche occupation and major evolutionary radiations.

A new species of the Ordovician horseshoe crab Lunataspis

“…Interestingly, a decrease in both the length of genal carapace extensions and lateral eye size is observed in eurypterid ontogeny (Lamsdell & Selden, 2013). As the generalized developmental trajectory for Xiphosura is recognized in both Belinurina and Limulina (Lamsdell, 2021a;Bicknell et al 2022) it is possible that Lunataspis, which resolves as the basalmost xiphosuran outside of the Belinurina and Limulina clades, is exhibiting a mixture of ancestral and derived ontogenetic trajectories and that the highly conserved developmental trajectory of Xiphosura developed somewhere within its stem lineage.…”

“…This traditional narrative has been overturned in recent years, with extinct horseshoe crabs shown to have greater ecological and morphological diversity than modern forms (Lamsdell, 2016) and a number of xiphosuran clades exhibiting marked shifts in morphology linked to heterochronic shifts in development as they occupy non-marine environments (Lamsdell, 2021a, b). Despite these morphological and ecological changes, horseshoe crabs are thought to have maintained a consistent post-embryonic developmental trajectory (Lamsdell, 2021a;Bicknell et al 2022) and exhibit a neuroanatomy conserved at least since the Carboniferous (Bicknell et al, 2021b), making xiphosurans an important group for studying the patterns and drivers of mosaic evolution (Hopkins & Lidgard, 2012;Hunt et al 2015).…”

An earliest Triassic age forTasmaniolimulusand comments on synchrotron tomography of Gondwanan horseshoe crabs

“…Extending CFD studies to fossil xiphosurids will facilitate comparative studies of the hydrodynamic properties of the carapaces of extinct members of the clade, in addition to elucidating the effects of bizarre morphologies, such as the hypertrophied genal spines, on fluid flow. Such spines have been hypothesised to represent an adaptation to movement through unidirectional fluid flow in primarily freshwater or marginal marine environments ( Lamsdell, 2016 ; Lamsdell, 2021 ; Bicknell & Pates, 2019 ; Bicknell & Shcherbakov, 2021 ; Bicknell et al, 2022a ); CFD provides the most compelling method for evaluating the likelihood of this hypothesis. Due to compression of the fossils (consider Dubbolimulus peetae ) CFD models of compressed xiphosurids would need to be retro-deformed, likely using modern forms as a proxy for inflation, to account for taphonomic alteration.…”

Evolvability and Macroevolution: Overview and Synthesis

“…The extinct forms are often not simply extensions along existing morphogenetic lines but variations that might seem highly improbable given today's representatives, for example giant ground sloths (terrestrial and aquatic), rainforest-dwelling carnivorous kangaroos, sharks with coiled tooth arrays, uncoiled or spiny nautiloids, echinoids with periscope-like extensions, and so on (see Jablonski, 2020 for references; also Stubbs et al, 2013 andMelstrom &Irmis, 2019 on insectivorous andherbivorous Crocodylomorpha). Even the quintessentially static lineage, the horseshoe crabs, has undergone bursts of phenotypic diversification that pushed beyond their current limited repertoire, corresponding to invasion of new habitats (Bicknell et al, 2022;Lamsdell, 2016). Wagner (2010) elegantly makes this general point by comparing Cambrian and present-day arthropods, which exhibit similar disparities (despite the far more limited Cambrian sample!)…”