Rapid phenotypic evolution following shifts in life cycle complexity

Abstract

Life cycle strategies have evolved extensively throughout the history of metazoans. The expression of disparate life stages within a single ontogeny can present conflicts to trait evolution, and therefore may have played a major role in shaping metazoan forms. However, few studies have examined the consequences of adding or subtracting life stages on patterns of trait evolution. By analysing trait evolution in a clade of closely related salamander lineages we show that shifts in the number of life cycle stages are associated with rapid phenotypic evolution. Specifically, salamanders with an aquatic-only (paedomorphic) life cycle have frequently added vertebrae to their trunk skeleton compared with closely related lineages with a complex aquatic-to-terrestrial (biphasic) life cycle. The rate of vertebral column evolution is also substantially lower in biphasic lineages, which may reflect the functional compromise of a complex cycle. This study demonstrates that the consequences of life cycle evolution can be detected at very fine scales of divergence. Rapid evolutionary responses can result from shifts in selective regimes following changes in life cycle complexity.

Multiple paedomorphic lineages of soft-substrate burrowing invertebrates: parallels in the origin of Xenocratena and Xenoturbella

“…The facultative-burrowing adult Xenocratena, therefore, demonstrates early stages of paedomorphic evolution, whereas obligate infaunal Pseudovermidae instead demonstrate its 'terminal stages', when adult animals closely resemble early postlarval stages of other aeolidacean nudibranchs [22,80]. Well-established examples from groups of vertebrates show that an irreversible fixation of originally facultative/intraspecific paedomorphic traits [58] is part of the evolutionary process [81]. Additionally, in the present analysis we also recovered parallel softsubstrate related paedomorphic simplification in another burrowing aeolidacean family, Embletoniidae (Fig 1), which possesses such definite signs of paedomorphosis as the presence of a small oral veil instead of oral tentacles and only a few cerata.…”

Terrestriality constrains salamander limb diversification: Implications for the evolution of pentadactyly

“…For some traits, this can produce developmental constraints that force a phenotypic trade‐off between life stages. However, ecological and developmental constraints across ontogeny can be lifted through metamorphosis (Moran, ; Wilbur, ) or by losing life cycle stages (Bonett & Blair, ; Bonett, Phillips, Ledbetter, Martin, & Lehman, ). Shifts in life cycle complexity should also impact the relationships among traits, but few studies have addressed this question in a phylogenetic context.…”

Testing the evolutionary constraints of metamorphosis: The ontogeny of head shape inTriturusnewts

“…As noted before, during metamorphosis some morphological structures are transformed, whereas other remain relatively unchanged or highly integrated across stages (Bonett and Blair ; Bonett et al. ). Body form and head shape in salamanders can be characterized as traits that undergo a different amount of changes during metamorphosis.…”

“…For the head shape, high within group variance and increased disparity were found at the metamorphosed stage, whereas the body shape was more canalized and conserved. As noted before, during metamorphosis some morphological structures are transformed, whereas other remain relatively unchanged or highly integrated across stages (Bonett and Blair 2017;Bonett et al 2018). Body form and head shape in salamanders can be characterized as traits that undergo a different amount of changes during metamorphosis.…”

“…Therefore, for both the axial skeleton and the limbs, there is a trade-off among contrasting func-tional demands between swimming and terrestrial locomotion (Gvoždik and Van Damme 2006). Increased evolvability coupled with elimination of one phase, aquatic or terrestrial (and therefore elimination of metamorphosis) is demonstrated for salamander body form (Bonett and Blair, 2017;Bonett et al 2018). Unlike the axial and limb skeleton, metamorphosis, by large-scale remodeling of cranial skeleton, dissociates specialized aquatic larval and terrestrial juvenile structures, allowing exploitation of contrasting environments.…”