Review

Evolutionary innovation and ecology in marine tetrapods from the Triassic to the Anthropocene

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Science  17 Apr 2015:
Vol. 348, Issue 6232, aaa3716
DOI: 10.1126/science.aaa3716

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Similar shapes inhabit the sea

Over biological history, several different groups of vertebrate tetrapods have reinvaded the marine environment. Although these groups are widely distributed among reptiles, mammals, amphibians, and birds, the shapes they have evolved are remarkably similar. Kelley and Pyenson review the literature on marine vertebrate groups over time and describe the innovations that facilitated the evolution of these marine forms, the environmental conditions that selected for such convergence of form, and the threats they face from future environment change.

Science, this issue 10.1126/science.aaa3716

Structured Abstract

BACKGROUND

More than 30 different lineages of amphibians, reptiles, birds, and mammals have independently invaded oceans ecosystems. Prominent examples include ichthyosaurs and mosasaurs during the Mesozoic (252 to 66 million years ago) and penguins and sea otters during the Cenozoic (66 million years ago to the present). In today’s oceans, marine tetrapods are ecologically important consumers with trophic influence disproportionate to their abundance. They have occupied apex roles in ocean food webs for more than 250 million years, through major changes in ocean and climate, and through mass extinctions. Major paleontological discoveries in the past 40 years have clarified the early land-sea transitions for some marine tetrapods (e.g., whales, sea cows), although the terrestrial origins of many lineages remain obscure. Incipient invasions appear frequently in marine tetrapod history, but such early transitions account for only a small proportion of the total fossil record of successful marine lineages, which in some cases persist for hundreds of millions of years.

ADVANCES

Marine tetrapods provide ideal models for testing macroevolutionary hypotheses because the repeated transitions between land and sea have driven innovation, convergence, and diversification against a backdrop of changing marine ecosystems and mass extinctions. Recent investigations across a broad range of scales—from molecules to food webs—have clarified the phylogenetic scope, timing, and ecological consequences of these repeated innovations. Studies of the physiology and functional morphology of living species have illuminated the constraints and tradeoffs that shape the pathway of initial marine invasions. Comparative studies on muscle myoglobin concentration or the evolution of sex determination mechanisms, for example, have revealed rampant convergence for these adaptive traits in the marine realm. Exceptionally preserved fossils have also revealed insights into reproductive biology, soft tissue structures, and trophic interactions. Fossils provide critical baselines for understanding historical changes in marine communities and diversity through time, and these baselines remain vital for evaluating the ongoing and severe anthropogenic disturbance to marine tetrapod populations and marine ecosystems as a whole.

OUTLOOK

Technological advances in remote sensing and biologging will continue to provide crucial insights into the macroecology of marine tetrapods below the water’s edge. Field data, when combined with extensive vouchers represented in museum collections, provide the basis for integrative models of the function and ecology of these logistically challenging organisms. Placed in a phylogenetic comparative framework, these data can enable tests of hypotheses about macroevolutionary patterns. Although perpetually incomplete, new fossil discoveries continue to improve our understanding of the early land-sea transitions in lineages and reveal past ecologies that could not have otherwise been predicted. Emerging imaging, molecular, and isotopic techniques provide an opportunity to expand the investigational scope for studying extinct taxa and to inform our understanding of how living species evolved. Lastly, resolving the full evolutionary scope of marine tetrapod history provides context for the origins of modern ecological patterns and interactions, which are fundamentally being altered by human activities.

A unified view of marine tetrapod evolution.

Circles mark initial invasions of marine tetrapod groups. Extinct and extant lineages are denoted by open and solid circles, respectively (yellow, amphibians; green, nonavian reptiles; blue, birds; red, mammals). Top curve summarizes marine tetrapod fossil richness through time. Schematic limb drawings demonstrate convergent hydrodynamic forelimbs in marine tetrapods (top to bottom): sea lion, whale, penguin, sea turtle, mosasaur, ichthyosaur. Ma, millions of years ago.

Abstract

Many top consumers in today’s oceans are marine tetrapods, a collection of lineages independently derived from terrestrial ancestors. The fossil record illuminates their transitions from land to sea, yet these initial invasions account for a small proportion of their evolutionary history. We review the history of marine invasions that drove major changes in anatomy, physiology, and ecology over more than 250 million years. Many innovations evolved convergently in multiple clades, whereas others are unique to individual lineages. The evolutionary arcs of these ecologically important clades are framed against the backdrop of mass extinctions and regime shifts in ocean ecosystems. Past and present human disruptions to marine tetrapods, with cascading impacts on marine ecosystems, underscore the need to link macroecology with evolutionary change.

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