Bridging Micro- and Macro- Evolution In Tropical Fishes
Abstract
In marine environments, barriers to dispersal can be challenging to identify because they are often cryptic. Unlike terrestrial environments, where a mountain chain that is visible can physically separate two populations of animals, vast masses of water in the ocean make it challenging to pinpoint these barriers. Therefore, the impact of these barriers on the formation of new species in the ocean is still not well understood. While most marine populations have long been considered to be well connected via long-distance dispersal, molecular ecology studies are increasingly unveiling inconspicuous barriers that promote population divergence and ultimately speciation. The advent of genomic techniques that allow the generation of data for thousands of genes has provided an unprecedented opportunity to uncover marine barriers that were previously invisible using more rudimentary tools. This, in turn, has opened new avenues for understanding of how barriers to dispersal affect population connectivity in the marine environment. The overarching goal of my dissertation is to use genome-wide data to look for genetic patterns that correspond to such barriers, and to test for their effect at short-, intermediate- and long-term evolutionary scales, going through a continuum from micro- to macro-evolution, in a time span from thousands to millions of years.
At the short-scale, I examined two controversial cases of species delimitation. Species delimitation is a major question in biology and is essential for adequate management of organismal diversity. The first challenging case involves the red snappers in the Western Atlantic. Red snappers have been traditionally recognized as two separate species based on morphology: Lutjanus campechanus (northern red snapper) and L. purpureus (southern red snapper). However, recent genetic studies using few molecular markers failed to delineate these nominal species, lumping the northern and southern populations into a single species (L. campechanus). To evaluate if the populations of these fish represent one or two species, my project applied ca. 40,000 genome-wide markers of 178 individuals collected throughout the range of the two species and population and species delimitation analyses. Overall, my results supported the isolation and differentiation of these species, a result that confirmed the morphology-based delimitation scenario, highlighting the benefits of using genome-wide data in complex cases of species delimitation (Chapter I, published in Proc. Roy. Soc. B in 2019).
The second study case involves a species complex of silverside fishes (Chirostoma humboltianum group: Atherinidae) in the Central Mexico plateau. The humboltianum group represents a taxonomically-controversial species complex where previous morphological and molecular studies based on a few genes produced conflicting species delineation scenarios. I applied an integrative approach that considered multiple lines of evidence to investigate the species numbers and boundaries comprising this contentious group. I used ca. 33,000 molecular markers for 77 individuals representing the nine nominal species in the group, spanning their distribution range in the central Mexico plateau, in combination with morphologic and ecologic information. My findings are inconsistent with the morphospecies and ecological delimitation scenarios, identifying three to four species. This study provides an atypical example in which genome-wide analyses delineate fewer species than previously recognized on the basis of morphological data alone. It also highlights the influence of geologic history as a main driver of speciation in the group (Chapter II, published in BMC Eco. Evol. B in 2022).
At the intermediate- scale, I evaluated the influence of historical (e.g., geophysical events) and contemporary barriers (e.g., habitat gaps) hindering genetic flow among populations by studying the spatio-temporal phylogenetic concordance of co-distributed lineages. For this study, I investigated the comparative phylogeography of labrisomid blennies in the genus Malacoctenus. I generated data for ca. 28K genome-wide markers that were sequenced from over 500 individuals collected from 38 locations, representing 23 (out of 25) species of Malacoctenus. With this dataset, I assessed the effect of recognized historical (e.g., the rising of the Isthmus of Panama) and contemporary barriers (e.g., sandy gaps) in the Tropical Eastern Pacific (TEP) and the Tropical Atlantic (TA) biogeographic realms. These blennies represent an ideal system to test the effect of such barriers as they are strongly associated with rocky habitats and coral reefs. Therefore, subtle habitat disruptions may lead to genetic isolation. At the micro-evolutionary scale, the observed population structure patterns identified the Sinaloan and Central American breaks as the major breaks in the TEP; and the Bahamas and Eastern Caribbean breaks as key barriers disrupting connectivity in the TA. All in all, the effect of these breaks varies across species, suggesting that species-specific traits (e.g., habitat preference), also greatly influence their dispersal capabilities. My study identified five instances where marine barriers promoted the diversification of independent evolutionary lineages that could potentially represent species complexes. Some of them supported by evidence of population differentiation from previous morphological analyses as well as by my geometric morphometric analyses. Major environmental variables driving population differentiation in the TEP are depth, temperature, chlorophyll altogether with spatial components, while in the TA suspended particle matter also influences diversification.
At the long-term scale, my results suggest that depth is a primary driver of speciation in the TEP, leading to niche divergence between tide pool- and reef-associated clades. In contrast, in the TA, patterns of environmental association appeared more intricate, where depth, temperature, chlorophyll and physical features significantly contributing to speciation in this region. Finally, our time-calibrated analyses at macroevolutionary scales elucidated an Eastern Atlantic origin of the clade followed by an east-to-west dispersal. Although the historical break attributed to the rise of the Isthmus of Panama had a substantial influence on the evolutionary history of the genus, our analyses demonstrate that it did not triggered synchronous cladogenetic events. In summary, by using a combination of population genomics, comparative phylogeography, phylogenomics, seascape genomics, and geometric morphometric approaches, this study highlights major contemporary and historical barriers hindering population connectivity in the TEP and TA biogeographic regions, enhancing our understanding of the forces and processes generating new species in marine systems (Chapter III, to be submitted for publication).
All in all, my thesis highlights that the use of genome-wide data provides unprecedented resolution to unveil patterns of genetic structure, commonly unraveling cryptic diversity, and the opportunity to address species delimitation problems. By uncovering the spatio-temporal genetic patterns of fishes along the evolutionary continuum, my dissertation provides novel insights into the evolutionary and biogeographic history of marine and freshwater Neotropical fishes. Overall, my dissertation not only helps to understand the evolutionary history of the species under study, but more generally, elucidate factors driving evolutionary process in the marine realm, ranging from population-level scales, to speciation, to higher level relationships among groups.
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