Worm sperm

You may have never thought about what feature distinguishes males from females. After all, in mammals the differences are often clear to us. In other groups too, the differences between male and female traits are often conspicuous. But, there are many species where male and female reproductive organs are both present in the same individual. Even in these species we can tell male parts from female parts.

To distinguish male from female we look at the relative size of the sex cells or gametes. Males produce the smaller gametes (e.g. sperm) and females produce the larger gametes (e.g. eggs). This difference in the size of the gametes is known as anisogamy, which essentially means without ("an") the same ("iso") gametes ("gamy"). 

The converse of anisogamy is isogamy. Species that are isogamous are very rare now, but this is thought to be the ancestral condition. As in anisogamous species where fertilisation only occurs when egg and sperm meet, fertilisation cannot occur in isogamous species unless the gametes of two different mating types meet. In isogamous species mating types are are referred to by various names, such as "+" and "-", in place of male and female.

The origins of anisogamy are unclear, but we have a pretty good explanation for why it evolved. Each gamete an individual produces costs energy and it must be stocked with additional reserves so that the zygote can complete development and start acquiring it's own energy. In isogamy, each member of a pair contributes half the energy to produce a viable offspring. In anisogamy, the cost is overwhelmingly paid by one of the mating types.

Investing almost nothing in individual gametes comes with a huge advantage, vastly more gametes can be produced increasing the number of offspring you can potentially produce. The more gametes an individual has the more fertilisations and individual can potentially achieve. Once one mating type gets far enough down the path of small gametes, its pair can't follow because that is likely to result in a zygote that doesn't have enough resources to survive.

It is relatively clear that fertilisation success has driven the evolution of males that produce more, small sperm. However, there are other aspects of sperm size and shape that appear to contribute to fertilisation success and these are surprisingly variable among and within species. Clear demonstrations that differences in sperm characteristics affect fertilisation success are rare, which makes a new paper in Evolution particularly interesting. 

Darren Johnson of the National Centre for Ecological Analysis and Synthesis, with Keyne Monro and Dustin Marshall of UQ (now both at Monash) looked at sperm traits in the broadcast spawning tubeworm, Galeolaria gemineoa. These worms can occur individually or in huge aggregations, leading to substantial variation in the concentrations of sperm and eggs in the wild. Because they don't leave their tubes, their options for increasing fertilisation success are limited relative to mobile species.

A colony of Galeolaria caespitosa, which are nearly identical to G. gemineoa (photo D. Semmens).

Groups of eggs from multiple females were exposed to the sperm of a single male at six different concentrations and two different ages. Fertilisation success was measured at the proportion of eggs that were undergoing normal development within each treatment. This is not a direct measure of fertilisation success because some embryos may have died very early due to genetic incompatibilities rather than the absence of fertilisation. However, it is a reasonable and practical proxy.

At high sperm concentrations, males that produced sperm with longer average tail length and smaller average head size achieved greater fertilisation success. In contrast, males that produced sperm with longer than average heads were favored at low sperm concentrations and older age. The results suggest that variation in sperm size and shape within a species may be preserved because different fertilisation environments favor contrasting sperm characteristics. 

The logistics of genetically assigning paternity prevented the authors from varying sperm competition environments. Had the sperm of multiple males been in competition to fertilise the eggs, different traits or trait combinations could have been favoured. While it is probably more realistic to pit the sperm of several males against each other, single male experiments still provide useful insights into selection on sperm traits.

An abbreviated version of this post also appears in the Research Highlights on the Australasian Evolution Society website.

References:

Johnson, D., Monro, K., & Marshall, D. (2013). The maintenance of sperm variability: Context-dependent selection on sperm morphology in a broadcast spawning invertebrate Evolution, 67 (5), 1383-1395 DOI: 10.1111/evo.12022

In the cave of the blind, the no-eyed crab is king

Cave dwelling creatures are often blind. The prevailing view is that, in such species, mutations in the visual system have little or no effect on fitness and vision is lost as these mutations gradually accumulate. There are several other types of characters that we can be reasonably confident are adaptations to life in caves, such as elaboration of structures for touch or smell. However, it is often hard identify which population cave adapted species are descended from and, therefore, how long ago they invaded caves. Without this information it has been hard to test ideas about the evolution of traits associated with life in the dark.

A cave form of the fish, Astyanax mexicanus, which is eyeless and unpigmented, traits typical in caves. It is a commonly used model species in studies of adaptation to cave environments (photo Wikimedia Commons).

Sebastian Klaus and colleagues from the National University of Singapore and Goethe University examined five species of freshwater crab in the genus Sundathelphusa, which occur on Bohol Island in the Philippines. Four species are only found in caves and the other has established several populations in caves. The repeated invasion of caves by the crabs has led to varying degrees of adaptation to life in the dark within the group. 

Freshwater crabs in the genus Sundathelphusa from Bohol Island. Thy are arranged from least cave adapted (top) to most cave adapted (bottom). From top to bottom the species are Sundathelphusa boex, S. vedeniki, S. urichi, S. sottoae and S. cavernicola (from Klaus et al. 2013).

The team used genetic data to estimate the time at which each species and population last shared a common ancestor. They then compared several features of cave-adapted crabs with their closest terrestrial relatives. Reductions in the visual system were just as pronounced as changes in cave-adapted features, indicating that evolution occurs at similar rates. The authors argue that this is a clear sign that eye loss is under directional selection because changes should appear more slowly if they are a result of selectively neutral mutations. 

They don’t speculate at all about what might favour eye-loss in the Bohol crabs, but hint in the introduction that it could be due to trade-offs between vision and other sensory systems. Trade-offs occur where increasing one aspect of fitness necessarily requires the reduction of fitness in another. If eyes are energetically costly to build and maintain then retaining functional eyes might prevent greater investment in other senses. Trade-offs are ubiquitous in biology and have been implicated in the loss of eyes in other cave dwelling species.

While I was doing research on this study I came across several creationist websites that argue cave adapted creatures are strong evidence that evolution is false because a trait is lost. According to them this shows evolution progressing in the wrong direction to what is predicted. They argue that evolution should progress towards more information and greater complexity. This is incorrect and shows, yet again, that creationists typically have a poor understanding of evolutionary theory.

The 'logic' of this argument is similar to the idea of a "Great Chain of Being", which pervaded early thinking about biology. This type of thinking is where we get several antiquated, but persistent terms, such as "missing link" and "highly evolved". It continues to dog evolution in the way that evolutionary information is often presented, such as the placement of organisms more closely related to us at the right or top of phylogenetic trees and at the end of textbooks.

The phylogeny of primates with humans at the top and less related groups at the bottom (from Wikipedia).

Linear descent was never part of Darwin's theory, nor was an increase in information ever a necessary assumption on which evolutionary theory rests. When you look at an evolutionary tree (like the primate tree above), all of the living species at the branch tips have an equally long evolutionary history. They are not descended from each other, they are descended from a common ancestor. You could say that they are equally evolved.

The first evolutionary tree drawn by Darwin over 20 years before the publication of On the Origin of Species.

Evolution doesn't prevent information from increasing, but contrary to the creationist claims it does predict that there will be strong limits on it. Both single trait and multi-trait trade-offs are thought to prevent organisms from becoming perfectly adapted. Single trait trade-offs occur where elaboration of a structure increases fitness in one environment, but reduces it in others. Multi-trait trade-offs occur where two or more structures are dependent on a shared finite resource.

Blind crabs are not evolving in the wrong direction. There is no wrong direction, they're just evolving under the constraint of trade-offs. Eye reduction and loss of pigmentation are not the only evolutionary changes that are occurring either. Other traits are becoming more elaborated, such as the length of their legs and the hairs on their claws, suggesting a multi-trait trade-off. This result is not only consistent with evolutionary theory, but expected.

An abbreviated version of this post is published on the Australasian Evolution Society website in the Research Highlights section.

Reference

Klaus, S., Mendoza, J., Liew, J., Plath, M., Meier, R., & Yeo, D. (2013). Rapid evolution of troglomorphic characters suggests selection rather than neutral mutation as a driver of eye reduction in cave crabs Biology Letters, 9 (2), 20121098-20121098 DOI: 10.1098/rsbl.2012.1098

Physics versus biology

When I was in high school, my physics teacher drew a massive rectangle that took up almost the entire black board and proclaimed, "this is physics". He then drew a little rectangle inside the first one and proclaimed, "this is biology". The he made a tiny little smudge of chalk on one of the sides of the 'biology' rectangle and said, "this is chemistry, so you all should study physics because all the other major division of science are just sub-disciplines of physics".

Amusing as his performance was, there are many aspects of biology that cannot be directly or indirectly inferred from our understanding of physics. Notably, we would have never formulated the theory of evolution, which underpins our modern understanding of biology, if we had to rely on progress in physics alone. Clearly though, physics is important in shaping the evolution of particular traits. I've written many times about physics in biology, such as swimming in sharks (here), flight in albatross (here), the hammer strike of mantis shrimp (here) and the visual capability of giant and colossal squid (here and revisited here).

Almost all organisms that detect and use light do so in the same part of the spectrum, which is pretty much the same part of the spectrum we see in. Although many use slightly shorter wavelengths in the ultraviolet or slighter longer wavelengths in the infrared, no organisms that we know of use the huge parts of the spectrum in the radio, x-ray and gamma ray wavelengths. I've wondered why this is before, but Mathew Cobb wondered it out loud and got some interesting answers.

Evolution, climate change and coral

Increased carbon dioxide in the atmosphere poses several problems for organisms living in the marine environment. Increases in temperature and ocean acidification are the two best known and most worrying. In order to predict how climate change and ocean acidification will affect marine species, we need to know how they respond to these conditions. The effect of climate change on corals has attracted a lot of attention because of their importance for biodiversity.

We can't just expose corals to predicted conditions because corals of the future won't be naive to these environments and are likely to have evolved. We know that evolution can be extremely rapid, often within decades. Ignoring the potential for evolution to influence the effects of climate change on marine organisms could lead to inaccurate projections of the effects of climate change on extinction risk. Yet many authors are ignoring the effects of evolution and acclimation in making their predictions. 

The three-spine stickleback, Gasterosteus aculeatus has been documented adapting to freshwater conditions from saltwater ancestors in just 13 generations (photo Wikipedia)

In their 2007 paper, Hoegh-Guldberg, et al. dismiss the importance of evolution because "reef-building corals have relatively long generation times and low genetic diversity, making for slow rates of adaptation". But, long generation times are not present in all coral species and the response of corals to climate change is going to depend partly on their algal symbionts, which have short generation times. 

Unfortunately, the rates of evolution in corals and their symbionts are extremely poorly known. In terrestrial systems though, genetic variation for traits related to thermal performance is common and evolutionary responses to changing climate are typical. For instance, changes in allele frequencies consistent with responses to global warming have been documented in a number of insects, such as fruit flies and mosquitoes (e.g. Bradshaw & Holzapfel 2001, Umina et al. 2005).

Acclimation, or phenotypic plasticity, will also affect the way that corals respond to climate change. Plastic responses to the environment can occur within generations and across them. For instance, Donelson et al. (2011) looked at the tropical damselfish, Acanthochromis polyacanthus, and found that their offspring could completely compensate for the negative effects of higher temperatures. But, this only occurred when both they and their parents where reared at the same temperature.

The tropical damselfish, Acanthochromis polycanthus (photo Wikipedia)

There are indications that some acclimation is occurring in corals too. Under stress, corals expel their algal symbionts, which gives them the appearance of having been bleached. Coral reefs that experience greater variability in sea surface temperature and those that have recently been subjected to bleaching are less susceptible to bleaching. This greater resilience suggests that some acclimation to climate change is possible within short time-frames. 

A bleached coral in the foreground with an unbleached coral of the same species behind (photo Wikipedia)

We need a better understanding of how evolution and acclimation may influence the response of corals to climate change so that our predictions are accurate. But, we already know which direction things are probably going to go. John Pandolfi's work has shown that under historical climate change, diversity on corals reefs has declined and populations have moved to higher latitudes (e.g. Pandolfi et al. 2011, Kiessling et al 2012). 

Climate change is currently more rapid than previous episodes and this will limit the amount of adaptation that can occur. Corals are also already under significant pressure from other anthropogenic sources of stress that have resulted in substantial declines and changes in population composition. These pressures, too, will decrease the ability of corals to cope with the effects of climate change. By removing these pressures, we will give corals the best chance possible to adapt to a warmer and more acidic ocean.

Hoegh-Guldberg, O., Mumby, P., Hooten, A., Steneck, R., Greenfield, P., Gomez, E., Harvell, C., Sale, P., Edwards, A., Caldeira, K., Knowlton, N., Eakin, C., Iglesias-Prieto, R., Muthiga, N., Bradbury, R., Dubi, A., & Hatziolos, M. (2007). Coral Reefs Under Rapid Climate Change and Ocean Acidification Science, 318 (5857), 1737-1742 DOI: 10.1126/science.1152509  

Bradshaw, W., & Holzapfel, C. (2001). Genetic shift in photoperiodic response correlated with global warming Proceedings of the National Academy of Sciences, 98 (25), 14509-14511 DOI: 10.1073/pnas.241391498

Umina, P., Weeks, A. R., Kearney, M. R., McKechnie, S. W., & Hoffmann, A. A. (2005). A Rapid Shift in a Classic Clinal Pattern in Drosophila Reflecting Climate Change Science, 308 (5722), 691-693 DOI: 10.1126/science.1109523

Donelson, J., Munday, P., McCormick, M., & Nilsson, G. (2011). Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish Global Change Biology, 17 (4), 1712-1719 DOI: 10.1111/j.1365-2486.2010.02339.x

Pandolfi, J., Connolly, S., Marshall, D., & Cohen, A. (2011). Projecting Coral Reef Futures Under Global Warming and Ocean Acidification Science, 333 (6041), 418-422 DOI: 10.1126/science.1204794 

Kiessling, W., Simpson, C., Beck, B., Mewis, H., & Pandolfi, J. (2012). Equatorial decline of reef corals during the last Pleistocene interglacial Proceedings of the National Academy of Sciences, 109 (52), 21378-21383 DOI: 10.1073/pnas.1214037110

A wrinkly hypothesis

The aquatic ape hypothesis was first proposed 70 years ago by German pathologist Max Westenhöfer. The hypothesis has more recently championed by Elaine Morgan, most notably in her book The Aquatic Ape. But the hypothesis has not drawn a lot of attention in the literature and has been dismantled in various places (here's one that's pretty good). Essentially the hypothesis interprets certain features, such as human hairlessness, as adaptations to an aquatic environment.

In 2011 Changizi et al. published a paper arguing that water-wrinkled fingers are an adaptation to life in aquatic environments. A new paper, just published, purports to test this hypothesis. Kareklas et al. had test subjects soak their hands in 40°C water for 30 minutes. Then they got the subjects to move marbles from a source container that was either filled with water or dry. The performance of the wrinkly handed participants was compared to a control group that performed the same task without soaking their hands.

Their results showed that the wrinkly finger group completed the marble moving task 12% faster when the source container was filled with water. There was no difference between the two groups when it was dry. They argue that their study shows a clear advantage to having wrinkly fingers when manipulating submerged items. But, I find the experiment completely underwhelming as support for wrinkly fingers as adaptations.

Most obviously, participants had to soak their hands in 40°C water for 30 minutes in order to obtain the small advantage. If wrinkled fingers are important for manipulating submerged objects, it seems to take an inordinately long time for fingers to wrinkle. Moreover, prior research has shown that lower temperatures, which are more likely to be encountered by our ancestors, result in slower and less exaggerated finger wrinkling (reviewed in Wilder-Smith 2004).

Marbles are also particularly small and slippery when compared with almost all conceivable objects that a paleolithic primate would be interested in picking up. It would be far more compelling if they had shown that the performance advantage remained when other objects were manipulated underwater. Given the very small advantage for marbles, I strongly suspect that the advantage would disappear for a vast array of other items.

The proponents of the aquatic ape hypothesis will probably incorporate the new study into their lists of evidence for a close association with with water in our ancestors. But, like most of their evidence, it is little better than plausible speculation dressed up as a compelling theory that deserves attention. It's a great way to get your ideas attention in the popular press, it's a horrible way to do science. The inoculation for such adaptationist nonsense is, as always, Gould and Lewontin 1979. 

Kareklas, K., Nettle, D., & Smulders, T. (2013). Water-induced finger wrinkles improve handling of wet objects Biology Letters, 9 (2), 20120999-20120999 DOI: 10.1098/rsbl.2012.0999 

Changizi, M., Weber, R., Kotecha, R., & Palazzo, J. (2011). Are Wet-Induced Wrinkled Fingers Primate Rain Treads? Brain, Behavior and Evolution, 77 (4), 286-290 DOI: 10.1159/000328223 

Wilder-Smith, E. (2004). Water immersion wrinkling Clinical Autonomic Research, 14 (2), 125-131 DOI: 10.1007/s10286-004-0172-4

Evolution, the most fascinating science

There are many amazing evolutionary adaptations. Here is a short video documenting just one.

Carnival of Evolution #52

The Carnival of Evolution #52 is now up at the Genealogical World of Phylogenetic Networks. There are some interesting posts there from some excellent science writers.

Rapid speciation in starfish

Australian waters are extremely rich in starfish species. Indeed, a little over 15% of all known species of starfish occur in Australia. For at least two of these starfish, speciation occurred extraordinarily fast. At most, they became separated about 22 thousand years ago, but the best estimate for the timing of the split is about 6 thousand years ago.

We know that evolution can be very rapid (e.g. sticklebacks) and that sometimes this leads to speciation (e.g. cichlids). But, in these cases selection is probably acting on a small number of alleles that are already present in the population. What makes the starfish study so breathtaking is that there has been profound changes to life history in the two species, which likely involved selection on many morphological and physiological traits.

Puritz et al. looked at Cryptasterina pentagona and its sister species C. hystria. Like most starfish, C. pentagona has separate sexes and reproduces by 'broadcasting' sperm and eggs into the water column where fertilisation occurs. In stark contrast, C. hystria produces both sperm and eggs simultaneously, and it exclusively self-fertilises within its own body cavity. The embryos of C. pentagona develop in the plankton, while C. hystria broods its offspring within the gonad until they are ready to emerge as small starfish.

It takes an expert to distinguish Cryptasterina hystria (top) and C. pentagona (bottom) in the wild. In fact I've seen the bottom picture shown as C. hystria and C. pentagona, but I think I got it right (photo Jon Puritz).

Puritz et al. speculate that water temperature may have provided the selective pressure that favoured the evolution of the C. hystria life history. Viviparity, like that seen in C. hystria, has been documented in a number of other starfish species. And it is consistently associated with species that occur in colder water. The two Cryptasterina species are separated by about 375 kilometers, with C. pentagona in the warmer north and C. hystria to the cooler south.

The authors also argue that small population size may have selected for self-fertilisation. If there are so few individuals in the population that your gametes are unlikely to meet another individual's, it's better to fertilise your own than to not reproduce at all. It's expected that genetic variation in a population that self-fertilises should be very low. But, genetic variation in C. hystria is so low it suggests the whole species derived from very few individuals, perhaps just a single one.


The transition from broadcast spawning with planktonic larval development to self-fertilisation with larvae brooded within the gonad has occurred in another Cryptasterina species, C. pacifica. In the closely related genus Parvulastra, a similar transition has occurred too, but probably over 500 thousand years. This suggests that the genetic variation required for the dramatic shift in life history is widely present in the group of starfish to which the genera Cryptasterina and Parvulastra belong. But, the speed at which evolution has occurred is truly astonishing.

Parvulastra exigua, note its similarity to the Cryptasterina species (photo Museum Victoria).

Puritz JB, Keever CC, Addison JA, Byrne M, Hart MW, Grosberg RK, & Toonen RJ (2012). Extraordinarily rapid life-history divergence between Cryptasterina sea star species. Proceedings. Biological sciences / The Royal Society, 279 (1744), 3914-3922 PMID: 22810427

Carnival of Evolution #51

The Carnival of Evolution number 51 is up at 'The Stochastic Scientist'. My post on beak size in birds made the list.

Selection on beak size in birds

The rapid evolution in the size and shape of bird beaks provide some of the best demonstrations of evolution in action. A classic example is the work of Rosemary and Peter Grant in the 1980's on Darwin's finches in the Galapagos. They showed that both competition and climatic conditions influenced beak size through changes in the availability of different sized seeds.

Gould's famous drawing of four of the fifteen species of Darwin's finches ([1] the large ground finch, [2] the medium ground finch, [3] the small tree finch and [4] the green warbler-finch). The Grants work primarily on the medium ground finch population on the island of Daphne Major, which they've visited every year since 1973.

Larger seeds are more difficult to crack. In drought years when they become proportionally more common, the finches with larger beaks did better because they had access to food that other birds didn't. Similarly, when a large seed eating competitor arrived, the birds with smaller beaks did better because smaller seeds became proportionally more common as competition for them was weaker.

The medium ground finch, Geospiza fortis. The Grants showed that its beak rapidly evolved to larger sizes in drought years and smaller sizes when faced with greater competition from the bigger beaked large ground finch, G. magnirostris (photo Wikipedia).

Although bird's beaks are clearly strongly shaped by diet, they are not just used for getting and eating food. The size and shape of beaks has also been linked to their use in preening and song production. More recently, studies have found that beaks may also play an important role in thermoregulation. Bigger beaks radiate more heat and could also help birds to conserve water in drier environments.

My pet kakariki (Cyanoramphus novaezelandiae). His beak is perfectly adapted for causing trouble.

In 2010, Symonds and Tattersall found that bird beaks conformed with Allan's rule, which posits that the relative size of body extremities should be smaller in colder environments to reduce heat loss. Bird beaks are highly vascularised and uninsulated extremities that can exchange a substantial amount of heat with the environment. Symonds and Tattersall found that beaks were relatively smaller in birds living at higher latitude and elevation.

In a recently published paper, Greenberg et al. develop this idea further. They argue that in drier environments birds could dissipate heat through their beaks rather than using evaporative cooling, thus conserving water. They test the hypothesis by examining the beaks of two subspecies of song sparrow, Melospiza melodia, that occupy habitats that contrast markedly in summer temperatures.

The song sparrow, Melospiza melodia (photo Wikipedia)

The Atlantic song sparrow lives in dune scrub and salt marsh edges along the mid-Atlantic coast, while the eastern song sparrow is widespread in gardens and wild scrublands. The coastal habitat of Atlantic song sparrows has higher summer temperatures and the availability of freshwater is limited relative to the habitat of the eastern song sparrow. And, consistent with the hypothesis, Atlantic song sparrows have beaks that are ~13% larger than eastern song sparrows.

To further evaluate the hypothesis, Greenberg et al. brought song sparrows into the laboratory where they could measure heat loss by thermally imaging the birds at constant ambient temperatures. Both subspecies maintained their beaks at higher than ambient temperature and higher than their body temperature. Heat lost through the beak was 5.6 - 10% of total heat loss, despite it making up less than 2.5% of total surface area.

A thermal image of an Atlantic song sparrow at an ambient temperature of 29°C (image Greenberg et al. 2012)

--> The beaks of the Atlantic song sparrows dissipated 33% more heat than the eastern song sparrow. Most of this difference can be explained by beak size, but Atlantic song sparrows may also maintain their beaks at higher temperatures than eastern song sparrows. Greenberg et al. estimate that the greater "dry" heat loss means an Atlantic song sparrow would conserve 7.7% more water than an eastern song sparrow of similar size.

In another study, Greenberg and Danner surveyed the beak size of song sparrows across California. They found that differences in beak size were strongly explained by the climatic conditions in which the birds lived. As summers became hotter and drier, song sparrow beaks became larger. Contrary to Allen's rule, winter temperatures poorly explained beak size differences, suggesting that heat dissipation is under stronger selection than heat conservation in the song sparrow.

Taken together these three studies support the hypothesis that climate is a significant selective pressure on the evolution of bird beaks. They highlight a little appreciated fact of evolution, that traits are often under multiple selection pressures and phenotypes are likely to reflect comprises between them. However, unlike the work on Darwin's finches, it has not been established that climate related beak size differences influence fitness variation. So, the work is strongly suggestive, but it's not a closed case.

References:

Symonds, MRE, & Tattersall, GJ (2010). Geographical Variation in Bill Size across Bird Species Provides Evidence for Allen’s Rule The American Naturalist, 176 (2), 188-197 DOI: 10.1086/653666  

Greenberg R, Cadena V, Danner RM, & Tattersall G (2012). Heat Loss May Explain Bill Size Differences between Birds Occupying Different Habitats. PloS one, 7 (7) DOI: 10.1371/journal.pone.0040933  

Greenberg R, & Danner RM (2012). The influence of the California marine layer on bill size in a generalist songbird Evolution DOI: 10.1111/j.1558-5646.2012.01726.x

Curiosities of evolution - Part I: Birds and viviparity

Evolution by natural selection is often incorrectly thought of as an unbounded path to novelty. I was reminded, when writing about coelacanths and manta rays, that there are some traits that are curiously absent from some lineages. In particular, the birth of live offspring (viviparity) has independently evolved many times in a diverse range of taxa, but not in birds or, probably, any other dinosaur (birds are theropod dinosaurs). Many adaptive explanations have been proposed to explain why this might be the case.

There are many ways that live birth can occur and many ways that the mother can provide nourishment to her offspring. The extant coelacanths, for instance, are what's known as 'oviviviparous', because females retain their eggs within their body until their offspring hatch, at which point the mother gives birth. Manta rays too, are oviviviparous, but mothers supply extensive additional nutrition after their offspring hatch.

In oviviviparous animals, the yolk allocated to the egg can be the only nourishment that offspring receive. But, there is a continuum from total reliance on the yolk, through various amounts of additional nutrition supplied by the mother (matrotrophy), to examples where all nutrition is supplied by the mother without yolk. Matrotrophy can be achieved with or without a placenta, and sometimes in alien ways, such as the cannibalism of siblings and unfertilised eggs within the uterus. Animals that are considered 'truly' viviparous are often only those where matrotrophy is complete.

After the ray-finned fishes, birds are the most species-rich lineage of vertebrates, yet not one species produces live young. The available evidence suggests that all dinosaurs were also egg laying. This is curious because all other major vertebrate groups, with the exception of the agnatha, have multiple examples (at least 120) of the independent evolution of live birth. And, unlike the agnatha, birds have several of the traits thought to be required for viviparity, like internal fertilisation.

Many hypotheses have been proposed to explain the lack of viviparity among birds; flight and the hard-shelled egg are the two explanations that seem to best fit the data. Pterosaurs, like birds, flew and seem to have all been egg laying. And bird's eggs are relatively impermeable to gas exchange when compared to those lineages of reptiles that have evolved viviparity. Indeed, turtles and crocodilians have similar hard-shelled eggs and have also not evolved viviparity.

However, these two hypotheses aren't completely satisfying. The 'flight-as-a-constraint' hypothesis is contradicted by live birth in bats and doesn't explain why none of the many flightless birds and dinosaurs evolved viviparity. The 'egg-as-a-constraint' hypothesis hinges on oxygen being a limitation and the assumption that the eggshell cannot be eliminated through evolution. But birds lay their eggs well before oxygen limitation would become a problem for embryos. And the evolution of viviparity in other lineages seems to begin with a lengthening of the period that eggs are retained before they are laid, only later does the eggshell thin to increase oxygen availability.

Some authors have suggested that viviparity has not evolved because directional selection for egg retention must be absent in birds, or that there is selection against it. The argument behind this hypothesis is that many of the advantages that viviparity may confer are solved by other means in birds and viviparity may have negative effects on mothers. For instance, retaining eggs internally may reduce the predation risk for offspring by decreasing the amount of time they're highly vulnerable to predators. But conversely, it may increase the risk of predation for mothers because they must carry an extra weight that could reduce their ability to escape.

Here too, counter examples can be found. For instance, there may be a selective advantage of egg retention in some species where eggs are a small fraction of maternal body mass and external incubation is costly. Many seabirds travel long distances between nesting sites and feeding grounds and they are also often large relative to the size of the egg. This suggests that carrying the extra weight of an egg is a minor cost and that there may be an energetic advantage to reducing the period of external incubation.

Other authors have suggested that the reason egg retention is short in birds is that their body temperature is too high for developing embryos. The resting temperature of birds is nearly universally 40 - 41 °C, while the optimal incubation temperatures are between 34  °C and 38 °C. Body temperature may, therefore, be a physiological constraint on egg retention in birds. But, correlation is not causation. Optimal incubation temperatures may have evolved because they're the temperatures that eggs are normally incubated at, not because they're the maximum temperatures that embryos can tolerate.

To me, the body temperature hypothesis probably carries the most weight as an adaptive explanation, but it remains untested. And, although the lack of viviparity in birds cries out for an adaptive explanation, we should not assume that the presence of absence of particular traits is the result of adaptive mechanisms. Nevertheless, the lack of viviparity in birds and other dinosaurs is an interesting and unresolved evolutionary question.

References:

Blackburn, D. G., & Evans, H. E. (1986). Why are there no viviparous birds? The American Naturalist, 128 (2), 165-190 DOI: 10.1086/284552 

Anderson, D. J., Stoyan, N. C., & Ricklefs, R. E. (1987). Why are there no viviparous birds? A comment. The American Naturalist, 130 (6), 941-947 DOI: 10.1086/284757