The evolutionary origins of diadromy inferred from a time-calibrated phylogeny for Clupeiformes (herring and allies)

Abstract

One of the most remarkable types of migration found in animals is diadromy, a life-history behaviour in which individuals move between oceans and freshwater habitats for feeding and reproduction. Diadromous fishes include iconic species such as salmon, eels and shad, and have long fascinated biologists because they undergo extraordinary physiological and behavioural modifications to survive in very different habitats. However, the evolutionary origins of diadromy remain poorly understood. Here, we examine the widely accepted productivity hypothesis, which states that differences in productivity between marine and freshwater biomes determine the origins of the different modes of diadromy. Specifically, the productivity hypothesis predicts that anadromous lineages should evolve in temperate areas from freshwater ancestors and catadromous lineages should evolve in tropical areas from marine ancestors. To test this, we generated a time-calibrated phylogeny for Clupeiformes (herrings, anchovies, sardines and allies), an ecologically and economically important group that includes high diversity of diadromous species. Our results do not support the productivity hypothesis. Instead we find that the different modes of diadromy do not have predictable ancestry based on latitude, and that predation, competition and geological history may be at least as important as productivity in determining the origins of diadromy.

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

“…Monophyly of the genus Alosa has been repeatedly supported based on mitochondrial, nuclear and combined molecular data (Bowen et al, ; Faria et al, ; Lavoué et al, ; Li & Orti, ); however, divergence times and rates of evolution have been a subject of debate (Bentzen et al, ; Bloom & Lovejoy, ; Faria et al, ; Lavoué et al, ). Our time‐calibrated analyses (Figure ) retrieved a topology identical to the composition of the major clades.…”

“…Previous biogeographical studies that focused on large‐scale analyses of the clupeiforms suggested that the common ancestor of Alosa and Brevoortia might have originated in the western Atlantic Ocean, followed by subsequent eastward dispersal that established European groups of Alosa spp. (Bloom & Lovejoy, ; Lavoué et al, ). This hypothesis offers a parsimonious biogeographical scenario corroborated by the restricted present‐day distribution of Brevoortia on the Atlantic coast of the Americas.…”

“…The lineage of Alosa that remained in the landlocked Mediterranean Basin had to exhibit remarkable euryhalinity to be able to survive in the hypersaline environment at the beginning of the salinity crisis followed by the hyposaline conditions during the Lago Mare (= Lake Sea) event (Bianchi et al, ). Such a transition seems feasible for Alosa considering its high tolerance of a broad salinity gradient and the ability to adapt rapidly to freshwater environments in landlocked populations observed in extant species (Bloom & Lovejoy, ; Lavoué et al, ; Palkovacs et al, ; Velotta et al, ). Subsequent re‐establishment of the Mediterranean Sea–Atlantic Ocean connection, together with fragmentation of the greater Mediterranean |Basin into a series of landlocked seas (Black Sea, Sea of Azov, Caspian Sea and Aral Sea), would have subdivided the European Alosa complex into areas in which populations would have evolved in isolation, becoming endemic to their regions (Figure , node A).…”

“…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.…”

Genetic relationships between landlocked and coastal populations of Lycengraulis grossidens (Engraulidae) in south-eastern South America: evidence for a continental colonisation route with secondary transitions to the coastal region

“…Lycengraulis comprises one of these freshwater lineages, and is assumed to be a product of a marine incursion that occurred during the Miocene epoch in the paleo-environmental ecosystem known as the Pebasian Sea (which existed ,15 million years ago; Monsch 1998;Bloom and Lovejoy 2012). The Pebasian Sea was located in the area currently encompassing the Amazon basin, and consisted of brackish to freshwater salinities that drained north-migration has potential evolutionary consequences because the gene flow between migrants and residents tends to be reduced as a result of allopatric spawning (McDowall 2008;Chapman et al 2012;Bloom and Lovejoy 2014). Moreover, studies based on otolith chemistry (Mai et al 2014) have demonstrated the presence of a landlocked population of L. grossidens in the Parana Basin (Uruguay River; in areas as far as 1500 km from the sea).…”