Are developmental shifts the main driver of phenotypic evolution in Diplodus spp. (Perciformes: Sparidae)?

Abstract

Background Sparid fishes of the genus Diplodus show a complex life history. Juveniles have adaptations well suited to life in the water column. When fishes recruit into the adult population, individuals develop a radically differentiated shape that reflects their adaptation to the new benthic environment typical of the adult. A comparative analysis of ontogenetic trajectories was performed to assess the presence of divergence in the developmental pattern . By using a geometric morphometric approach, we investigated the pattern of shape variation across ontogenetic stages that span from early settlement to the adult stage in four species of the genus Diplodus . Landmarks were collected on the whole body of fishes to quantify the phenotypic variation along two well defined life stages, i.e. juvenile and adult. A comparative analysis of ontogenetic trajectories was performed to assess the presence of divergence in the developmental pattern. Subsequently, we investigated the patterns of integration and modularity as proxy for the alteration of the developmental processes. This have allowed to give an insight in morphological developmental patterns across ecologically and ontogenetically differentiated life stages and to investigate the process leading to the adult shape. Result Our results suggest that the origin of morphological novelties in Diplodus spp. arise from shifts of the ontogenetic trajectories during development. During the settlement phase, the juveniles’ morphological shapes converge towards similar regions of the morphospace. When the four species approach the transition between settlement and recruitment, we observe the lowest level of inter- and intra-specific disparity. After this transition we detect an abrupt shift of ontogenetic trajectories, i.e. the path taken by species during development, that led to highly divergent adult phenotypes. Discussion We suggest that the evolution of new ecomorphologies, better suited to exploit different niches (pelagic vs. benthonic) and reduce inter-specific competition in Diplodus spp., are related to the shift in the ontogenetic trajectory that in turn is associated to changes in modularity and integration pattern. Electronic supplementary material The online version of this article (10.1186/s12862-019-1424-1) contains supplementary material, which is available to authorized users.

A new method for quantifying heterochrony in evolutionary lineages

“…It seems that shifts in environmental occupation set these lineages along a heterochronic trajectory resulting in a directional bias (Gould 1982), whereby changes in the timing or rate of development produce innovative morphologies, the selection of which—mediated by the environment—result in increasingly specialized phenotypes. Heterochronic processes are known to be one of the primary ways by which morphological innovation (sensu Erwin 2015a, 2017) occurs (McNamara and McKinney 2005; McNamara 2012; Colangelo et al 2019), and it is the nonmarine xiphosurans that contribute the most to xiphosuran disparity and occupy novel regions of morphospace (Lamsdell 2016).…”

“…This model of adaptive radiation has been invoked as the dominant causal factor of major evolutionary events in Earth's history, including the Cambrian explosion (Erwin and Valentine 2013), invasion of freshwater ecosystems (Davis et al 2018), colonization of land (Benton 2010), and recovery from mass extinction events (Toljagić and Butler 2013). In turn, the innovation of phenotypes is recognized to occur through heritable alterations in the timing of an organism's development, a process known as heterochrony (McNamara and McKinney 2005; McNamara 2012; Colangelo et al 2019). Therefore, heterochronic processes result in new morphological characteristics that can allow organisms to exploit new environments and subsequently diversify.…”

Geometric morphometric analysis of body shape and size variations in hatchery-reared larvae of a tropical damsel fish, Dascyllus carneus Fischer, 1885

“…in their social systems, did not play a major role in the distribution of juvenile; and also not in the survival and mortality of an organism under wild conditions [30,[110][111][112] . This suggests that natural selection can have a positive effect in selecting those changes in the ontogenetic trajectories that lead to new morphological forms, which in turn reduce the intraspeci c competitions [31] . In the selection process, the DCTS is one of the crucial checkpoints for the survival of organisms where a substantial number of variations minimize intraspeci c competitions in the wild [113] .…”

“…Geometric morphometric tool has been effectively used for the quantitative statistical description of the organism's shape. Only limited reviews are available on the empirical expression of dynamic transformation patterns during the post-embryonic development of marine shes [12,13,17,[22][23][24][25][26][27][28][29][30][31] . Allometry, the covariation pattern between several morphological features or between size and shape measurements [32] , can be used to describe the evolutionary developmental history of the animal's growth trajectories [33] , which in turn contribute to morphological integration [34] .…”

Current Options for Visualization of Local Deformation in Modern Shape Analysis Applied to Paleobiological Case Studies

“…GM is being routinely used to address a wide spectrum of hypotheses. In particular, the use of shape analysis has been fruitfully coupled with phylogenetic comparative methods in order to explore patterns of convergence/divergence (Stayton, 2015;Castiglione et al, 2019), morphospace occupation (Santos et al, 2019), morphological integration (Piras et al, 2014;Sansalone et al, 2019), functional hypothesis (Oxnard and O'Higgins, 2009), and developmental growth (Angulo-Bedoya et al, 2019;Colangelo et al, 2019). All these studies share the same basic source of phenomenological interpretation: the shape change studied via shape analysis (very often GM).…”