Phylogenetic analysis of trophic niche evolution reveals a latitudinal herbivory gradient in Clupeoidei (herrings, anchovies, and allies)

Abstract

Biotic and abiotic forces govern the evolution of trophic niches, which profoundly impact ecological and evolutionary processes and aspects of species biology. Herbivory is a particularly interesting trophic niche because there are theorized trade-offs associated with diets comprised of low quality food that might prevent the evolution of herbivory in certain environments. Herbivory has also been identified as a potential evolutionary "dead-end" that hinders subsequent trophic diversification. For this study we investigated trophic niche evolution in Clupeoidei (anchovies, sardines, herrings, and their relatives) and tested the hypotheses that herbivory is negatively correlated with salinity and latitude using a novel, time-calibrated molecular phylogeny, trophic guilds delimited using diet data and cluster analysis, and standard and phylogenetically-informed statistical methods. We identified eight clupeoid trophic guilds: molluscivore, terrestrial invertivore, phytoplanktivore, macroalgivore, detritivore, piscivore, crustacivore, and zooplanktivore. Standard statistical methods found a significant negative correlation between latitude and the proportion of herbivorous clupeoids (herbivorous clupeoid species/total clupeoid species), but no significant difference in the proportion of herbivorous clupeoids between freshwater and marine environments. Phylogenetic least squares regression did not identify significant negative correlations between latitude and herbivory or salinity and herbivory. In clupeoids there were five evolutionary transitions from non-herbivore to herbivore guilds and no transitions from herbivore to non-herbivore guilds. There were no transitions to zooplanktivore, the most common guild, but it gave rise to all trophic guilds, except algivore, at least once. Transitions to herbivory comprised a significantly greater proportion of diet transitions in tropical and subtropical (<35°) relative to temperate areas (>35°). Our findings suggest cold temperatures may constrain the evolution of herbivory and that herbivory might act as an evolutionary "dead-end" that hinders subsequent trophic diversification, while zooplanktivory acts as an evolutionary "cradle" that facilitates trophic diversification.

Systematics of Clupeiformes and testing for ecological limits on species richness in a trans-marine/freshwater clade

“…Bayesian mtDNA and nDNA analyses placed Spratelloidinae sister to all remaining Clupeidae and mtDNA analyses placed Spratelloidinae with our outgroup. Previous molecular studies have also recovered Spratelloidinae as a distinct group and have most consistently placed this lineage sister to all remaining Clupeoidei (Lavoué et al, 2013(Lavoué et al, , 2014Bloom, Lovejoy, 2014;Egan et al, 2018). As such, including Spratelloidinae in either Dussumieriidae or Clupeidae renders these taxa as non-monophyletic.…”

“…Clupeiformes display a wide range phenotypic diversity, including miniaturized species that achieve a maximum size of 2 mm and large species reaching 300 mm TL (Whitehead, 1985b;Bloom et al in press). The group occupies an array of trophic guilds, such as planktivores, algivores, piscivores, molluscivores, and more (Egan et al, 2018). Clupeiformes also inhabit a broad spectrum of habitats, including open ocean, coastal areas, estuaries, and freshwater rivers and lakes.…”

“…Combined mtDNA and nDNA analyses suggested Pristigasteridae was sister to the Chirocentridae+Engraulidae, but with no statistical support (Bloom, Lovejoy, 2014). Most recently, using six nuclear genes, Egan et al (2018) supported Chirocentridae as sister to Engraulidae, but also recovered Pristigasteridae as nested within Clupeidae.…”

The Adaptive Evolution of Herbivory in Freshwater Systems

“…The evolution of herbivory in Terapontid fishes is more intuitive, as this process was driven by the transition into heterogeneous freshwaters . In Cleupeoid fishes, the evolution of herbivory was not driven by habitat transitions, but was instead driven by latitude (Egan et al 2018). These results support multiple transitions between freshwater and euryhaline habitats in the genus Poecilia (particularly in the subgenera Poecilia and Mollienesia), and I show that these transitions are related to the evolution of herbivory in the same species.…”

Delimitation of Alosa species (Teleostei: Clupeiformes) from the Sea of Azov: integrating morphological and molecular approaches

“…A time‐calibrated analysis of the concatenated coI – cytb data set (58 ingroup taxa, 1,099 bp) was performed in BEAST 2.4.6 (Bouckaert et al, ) under the birth–death model. Because there is uncertainty in the accurate identification of fossils as Alosinae or Alosa , a root node age was sampled from a uniform distribution over the range from 15 to 40 Myears ago (MYA) as estimated by the recent time‐calibrated analyses of the Clupeoidei (Bloom & Lovejoy, ; Egan et al, ; Lavoué et al, ). All tip ages represented by extant taxa were set to 0 MYA.…”