A new method for quantifying heterochrony in evolutionary lineages

Abstract

The occupation of new environments by evolutionary lineages is frequently associated with morphological changes. This covariation of ecotype and phenotype is expected due to the process of natural selection, whereby environmental pressures lead to the proliferation of morphological variants that are a better fit for the prevailing abiotic conditions. One primary mechanism by which phenotypic variants are known to arise is through changes in the timing or duration of organismal development resulting in alterations to adult morphology, a process known as heterochrony. While numerous studies have demonstrated heterochronic trends in association with environmental gradients, few have done so within a phylogenetic context. Understanding species interrelationships is necessary to determine whether morphological change is due to heterochronic processes; however, research is hampered by the lack of a quantitative metric with which to assess the degree of heterochronic traits expressed within and among species. Here I present a new metric for quantifying heterochronic change, expressed as a heterochronic weighting, and apply it to xiphosuran chelicerates within a phylogenetic context to reveal concerted independent heterochronic trends. These trends correlate with shifts in environmental occupation from marine to nonmarine habitats, resulting in a macroevolutionary ratchet. Critically, the distribution of heterochronic weightings among species shows evidence of being influenced by both historical, phylogenetic processes and external ecological pressures. Heterochronic weighting proves to be an effective method to quantify heterochronic trends within a phylogenetic framework and is readily applicable to any group of organisms that have well-defined morphological characteristics, ontogenetic information, and resolved internal relationships.

The phylogeny and systematics of Xiphosura

“…The phylogeny of Xiphosura was analyzed through an expanded version of the latest iteration of the chelicerate character matrix of Lamsdell (2020) , derived incrementally from previous analyses of broader euchelicerate relationships ( Lamsdell, 2013 ; Lamsdell, 2016 ; Lamsdell & McKenzie, 2015 ; Lamsdell et al, 2015 ; Selden, Lamsdell & Liu, 2015 ). The matrix comprises 259 characters coded for 158 taxa and is available in the online MorphoBank database ( O’Leary & Kaufman, 2012 ) under the project code p3497 (accessible from https://morphobank.org/index.php/Projects/ProjectOverview/project_id/3497 ) as well as in the Supplementary Information .…”

“…Morphological terminology for character definitions follows Selden & Siveter (1987) , Lamsdell (2013) , Lamsdell (2016) and Lamsdell (2020) –see Fig. 3 for a basic overview of major terms.…”

“…Tree inference was performed as in Lamsdell (2020) , via Bayesian inference through Markov-Chain Monte Carlo analyses implemented in MrBayes 3.2.7a ( Huelsenbeck & Ronquist, 2001 ). The dataset was analyzed through four independent runs of 100,000,000 generations and four chains each under the maximum likelihood model for discrete morphological character data with gamma-distributed rate variation among sites (Mkv + Γ: Lewis, 2001 ).…”

“…More recently, phylogenetic analysis of extant and fossil limuloid xiphosurans suggested that molecular rate estimates for the living species were significantly underestimating their divergence times ( Lamsdell & McKenzie, 2015 ). Subsequent analyses have expanded the taxon sampling to encompass all major xiphosuran clades in order to study the relationship between ecological occupation and morphological disparity ( Lamsdell, 2016 ) and ecological occupation and heterochronic trends ( Lamsdell, 2020 ). These investigations suggested that a number of xiphosuran genera were para- or polyphyletic, as well as inferring major revisions to xiphosuran higher-level taxonomy.…”

“…While the higher-level taxonomy of Xiphosura was updated to accommodate the phylogenetic topology ( Lamsdell, 2016 ), no in-depth diagnoses of the higher taxa was attempted, and no diagnostic revision of genera was undertaken. Given that many paleobiological meta-analyses operate at the genus level ( Hendricks et al, 2014 ) and that Xiphosura is a clade of particular interest to evolutionary biologists ( Renwick, 1968 ; Barthel, 1974 ; Fisher, 1981 ; Fisher, 1984 ; Fisher, 1990 ; Mattei et al, 2010 ; Faurby et al, 2011 ; Haug et al, 2012 ; Kin & Błażejowski, 2014 ; Moreau et al, 2014 ; Göpel & Wirkner, 2015 ; Lamsdell, 2016 ; Lamsdell, 2020 ; Lamsdell, in press ; Periasamy, Ingole & Meena, 2017 ; Shingate et al, 2020 ), it is critical that the lower-level taxonomy of horseshoe crabs also be revised in line with their phylogenetic relationships.…”